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Paleoparasitology of Chagas Disease - a Review

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Paleoparasitology of Chagas Disease - a Review Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 104(Suppl. I): 9-16, 2009 9 Paleoparasitology of Chagas disease - A Review Adauto Araújo1/+, Ana Maria Jansen2, Karl Reinhard3, Luiz Fernando Ferreira1 1Escola Nacional de Saúde Pública-Fiocruz, Rua Leopoldo Bulhões 1480, 21041-210 Rio de Janeiro, RJ, Brasil 2Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz-Fiocruz, Rio de Janeiro, RJ, Brasil 3School of Natural Resource Sciences, University of Nebraska-Lincoln, Lincoln, USA One hundred years since the discovery of Chagas disease associated with Trypanosoma cruzi infection, grow- ing attention has focused on understanding the evolution in parasite-human host interaction. This interest has featured studies and results from paleoparasitology, not only the description of lesions in mummified bodies, but also the recovery of genetic material from the parasite and the possibility of analyzing such material over time. The present study reviews the evidence of Chagas disease in organic remains excavated from archeological sites and discusses two findings in greater detail, both with lesions suggestive of chagasic megacolon and confirmed by molecular biology techniques. One of these sites is located in the United States, on the border between Texas and Mexico and the other in state of Minas Gerais, in the Brazilian cerrado (savannah). Dated prior to contact with Europeans, these results confirm that Chagas disease affected prehistoric human groups in other regions outside the Andean altiplanos and other transmission areas on the Pacific Coast, previously considered the origin of T. cruzi infection in the human host. Key words: paleoparasitology - paleoepidemiology - Chagas disease - ancient DNA - mummies - Trypanosoma cruzi Although Chagas disease transmission by Triatoma Trypanosomatids in mammals infestans has been eliminated from Brazil, the remain- Trypanosomatids are flagellate protozoa of the Ki- ing chronic cases still pose a serious problem, espe- netoplastida order, which includes both free-living or- cially in regions of the country where access to health ganisms and parasites. The latter comprise monogenetic care is more difficult. Chagas disease brings suffering and digenetic organisms with extranuclear circular DNA and death for many people in Latin America, where peculiarly arranged as maxi and minicircles. Trypanoso- many young adults still die early from cardiac lesions. matids of mammals provide an excellent example of how Brazilian health authorities have been alert to the oc- molecular paleoparasitology can shed light on epidemio- currence (mainly in the Amazon) of oral transmission logical and biological questions. Trypanosomatids are through the ingestion of foods contaminated with vec- very old eukaryotic organisms that probably diverged tor-derived infective forms (metacyclic forms) (Dias from the first eukaryotes soon after their association & Coura 1997, Roque et al. 2008). These cases of oral with the mitochondrion. transmission, occurring as outbreaks, are characterized Kinetoplastida are characterized by the presence of by the appearance of acute and sometimes quite severe kDNA or kinetoplast DNA, an extranuclear DNA net- forms of the disease. work formed by circular molecules, maxi and minicir- Chagas disease must also have been a serious prob- cles and that correspond to the parasite mitochondrial lem among prehistoric populations, especially if the genome, localize near the flagellate’s basal body. possibility of sudden death in young adults and the The Kinetoplastida include the Trypanosomatidae consequences of the chronic phase, whether intestinal family, an exclusively parasitic taxon that infects a or cardiac is considered. Several paleoparasitological wide range of animals and plants, and the Bodonidae findings point to Chagas infection in various regions family, that includes parasitic and exclusively free- of the Americas, as well as cases of severe cardiac and living organisms. megacolon lesions. This article discusses the evolution- Trypanosoma cruzi is characterized by important ary aspects of trypanosomatids and their transmission to heterogeneity and biological plasticity. These peculiari- humans in prehistoric times in the Americas. ties were already observed in the pioneering studies by Carlos Chagas and Brumpt and represent an unresolved epidemiological conundrum to this day. The heterogene- ity of T. cruzi that is expressed by various markers, as biological (differences in the infection pattern in mice and growth in axenic culture, differences in competence when colonizing culture cells and resistance to chemo- Financial support: CNPq, FAPERJ, FIOCRUZ, CAPES, Fulbright therapeutic agents, among others), biochemical and mo- Commission + Corresponding author: [email protected] lecular, result in the wide distribution in nature and in Received 12 March 2009 distinct epidemiological scenarios. In fact, T. cruzi is ca- Accepted 1 June 2009 pable of infecting more than a hundred species of mam- online | memorias.ioc.fiocruz.br 10 Paleoepidemiology of T. cruzi • Adauto Araújo et al. mals and, within these, nearly all the tissues. Another ago, when South America separated from Africa (Haag important aspect of T. cruzi biology relates to the para- et al. 1998). According to several authors (Rothhammer site’s multiple transmission mechanisms: transfusional, et al. 1985, Coimbra Jr 1988, Stevens & Gibson 1999), congenital, oral and by contamination of the skin and humans were introduced into the T. cruzi transmission mucous membranes with triatomine feces carrying the cycle after domestication of plants and animals and infective metacyclic trypomastigotes forms. T. cruzi is acquisition of sedentary habits. Thus, according to the also a generalist parasite in relation to the vector, since widely accepted theory on the origin of Chagas dis- the protozoan infects dozens of triatomine species from ease in humans, approximately 8,000-6,000 years ago the Reduviidae family. The parasite’s biological plastic- the Andean peoples began domesticating small rodents ity results in transmission cycles in nature that are char- (Cavia sp.) for consumption and for rituals. The animals acterized as multivariable, complex and peculiar on a were raised inside the houses, where they attracted he- temporal and spatial scale. This complexity means that matophagous insects, specifically T. cruzi vectors. The over time, humans have probably contacted the parasite beginning of grain storage and the resulting attraction on different occasions and through different routes, de- of grain-eating mammals also presumably played an im- pending mainly on how they interacted with the envi- portant role in this process. The triatomine vectors of T. ronment, i.e., how they were exposed to infection. cruzi, especially the T. infestans species, found optimum Since the pioneering work by Carlos Chagas, re- conditions in the mud and daub human dwellings for col- searchers have attempted to establish a correlation be- onization and blood meals from both humans and their tween some genotypic or phenotypic characteristic in the domestic animals. Importantly, adaptation by a triatom- parasite and the disease’s profile and characteristics relat- ine to a new habitat, in this case human dwellings, is and ed to local epidemiology, the vector, or animal reservoirs. probably was a very long process that includes genetic Although many aspects of T. cruzi biology and ecology simplification (Schofield et al. 1994) - it is interesting have been elucidated, numerous questions still remain to recall that sylvatic colonies of T. infestans have never unanswered and no one has ever consistently associated been described in Brazil. a given type of isolate to the disease or its epidemiology. The T. infestans species probably became domicili- We do know that T. cruzi presents a multiclonal popu- ated at that time, spreading to a major extent with the lation structure, with high genetic diversity. The first bio- help of human migrations to other parts of South Ameri- chemical characterization studies analyzing different iso- ca, including the opposite side of the Andean Cordillera. lates of the parasite identified three types of zymodemes, The process intensified after the arrival of Europeans two of which (Z1 and Z3) were associated in Brazil with and Africans on the continent, with the spread of precar- the sylvatic transmission cycles, while Z2 was associated ious human dwellings made of “mud and daub”, where with the domestic transmission cycle below the Amazon the vector found prime conditions for colonization in the (Miles et al. 1977, 1978). Molecular tools grouped dif- cracks and crannies in the walls (typical of this kind of ferent sub-populations of the parasite into two distinct construction). According to this theory, Chagas disease and phylogenetically distant genotypes. These genotypes thus originated in the Andean Region, in prehistoric were termed T. cruzi I and T. cruzi II and correspond, populations 8,000-6,000 BP, reaching other regions of respectively, to Z1 and Z2. More recently, six sub-popu- the Americas beginning with the European colonial pe- lations were described in the taxon: TCI and TCII, with riod (Dias & Coura 1997). the latter genotype subdivided into TCIIa, TCIIb, TCIIc, It was thought that in what is now Brazil, T. cruzi TCIIe and TCd that excepting TCIIb, having originat- would never have been a problem for the indigenous ed in part from two hybridization events in the parasite populations, since the
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