The Sylvatic
Cycle of Trypanosoma cruzi: a Still Unsolved Puzzle
Suppl. I:
203-204
Ana Maria
Jansen/+, Ana Paula Santos de Pinho, Cristiane Varella
Lisboa, Elisa Cupolillo*, Regina Helena Mangia**, Octavio Fernandes**
Departmento de
Protozoologia *Departmento de Imunologia ** Departamento de Medicina
Tropical,
Instituto Oswaldo Cruz, Av. Brasil 4365, 21045-900 Rio de
Janeiro, RJ, Brasil
Key words:
Trypanosoma cruzi - sylvatic cycle
Despite its
clonal structure (Miles & Cibulskis 1986, Tibayrenc & Ayala
1986) Trypanosoma cruzi presents an extreme variability
and the seminal studies described the pleomorphism of this
tripanosomatid. The slender blood forms have been taken for immature
forms or male gametes and the large blood forms, as mature forms or
female gametes (Chagas 1909, Brumpt 1912). Since then, all attempts made
to correlate biological, biochemical and morphological parameters of the
parasite with the course of the experimental infection or with the
different aspects of Chagas disease, has led to controversial results.
Nevertheless, the study of enzyme electrophoresis profiles defined three
major subpopulations (zymodemes) in Brazil, associated to domestic (ZII)
or sylvatic transmission cycle (ZI and ZIII) (Barrett et al. 1980). More
recently molecular markers separated two distinct and major
phylogenetically lineages in T. cruzi also associated to the
domiciliar transmission cycle (lineage 1), and to the sylvatic
transmission cycle (lineage 2) (Souto et al.1995, Zingales et al. 1997,
Fernandes et al. 1998).
However, what is
the so-called "T. cruzi sylvatic transmission cycle"? It is well
known that naturally infected mammals and bugs can be found in almost
any sylvatic ecotope, but very little is known about the kinetics of the
transmission of T. cruzi among its vertebrate and invertebrate
hosts in the natural environment. The performed surveys reflect a cross
sectional analysis of the enzooty, and do not consider the peculiarities
of the interaction of the parasite with a given host. The studies of the
interaction of T. cruzi with marsupials, considered to be the
most important and probably the most ancient reservoirs, has yielded a
series of new data on the biology and ecology of this flagellate. This
is exemplified by the cycle undertaken by the parasite in the lumen of
the scent glands of Didelphis marsupialis, where the protozoan
multiplies as epimastigotes and differentiates into metacyclic forms
(Deane et al. 1984). The extracellular multiplication cycle of T.
cruzi in the scent glands of the opossum D. marsupialis
evidences that, besides being a reservoir host, this species can
also be a vector of T. cruzi. Another peculiarity of the
interaction of T. cruzi with marsupials, is the effective control
of the infection by D. marsupialis and Philander opossum.
Moreover, D. marsupialis are able to rapidly control and even
eliminate infections with T. cruzi Y strain, while maintaining
other strains indefinitely without any significant tissue lesion (Deane
et al. 1984). P. opossum, on the contrary, maintains both types
of strains (Pinho et al. 1993).
Studying the
circulation of T. cruzi among triatomine vectors, P.
opossum and D. marsupialis captured in a same area of the
Atlantic Coastal Rainforest we observed that 50% of the marsupials and
bugs, were naturally infected. The biological, biochemical and molecular
characterization of the T. cruzi isolates defined two groups,
associated mainly to P. opossum or D. marsupialis. The
collected bugs (Rhodnius prolixus) were most probably involved
with the transmission of the parasite among D. marsupialis, since
their T. cruzi isolates displayed similar biological, biochemical
and molecular characteristics. Furthermore although P. opossum and D.
marsupialis occupy the same sylvan habitat exclusively D.
marsupialis frequents and even colonize human dwellings and
therefore was considered as a link between the sylvan and domestic
transmission cycles but it was observed that only P. opossum
harbored T. cruzi lineage 1 parasites. The presence of
lineage 1 in D. marsupialis is rare (Zingales et al. 1998,
Fernandes et al. 1999). These findings and our previous observations
that in experimental conditions P. opossum do not select
subpopulations of T. cruzi, contrary to D. marsupialis,
strongly suggested two independent transmission cycles occurring between
these two marsupial species that live sympatrically. Furthermore suggest
an explanation to the absence oh human infection in the studied area.
Going further in
our observations we decided to study, in another area of the Atlantic
Coastal Rainforest, a greater range of hosts: sloths, rodents,
marsupials and golden lion tamarins (Leonto-pithecus rosalia), an
endangered primate species included in a conservation program. There, we
observed a completely distinct enzootic picture since L. rosalia
was the most infected species, (52%) in comparison to the marsupials
(5.3 %) and rodents (18%). All L. rosalia isolates were typed as
belonging to lineage 1. On the other hand, all isolates derived from the
other mammals including one sloth isolate, were typed as belonging to
lineage 2. The only bug found in that area, a Triatoma vitticeps,
was infected with flagellates which were in lineage 1 (Lisboa et al.
1996). Our observations suggest that dispersion of T. cruzi in
the sylvatic environment can occur through simultaneous distinct and
independent tansmission cycles which are ruled by still unknown factors,
not including e.g. forest strata, since golden lion tamarins and sloths
are both arboreal animals. Moreover, the sylvatic transmission cycle is
much more complex than assumed up to now. Therefore, no generalization
or prediction should be made in an enzootical study of parasites and
each ecotope should be considered as a unique system by every program
which include managing of the sylvatic environment. Several pathogenic
trypanosomatids of mammals infect a broad range of vertebrate and
invertebrate hosts circulating therefore among dozens of different
species of insects and mammals in distinct ecotopes. Consequently, the
outbreaks of the diseases are drive by diverse factors such as the
presence of carriers, wildlife reservoirs, concentration of infected
animals and vectors, husbandry practices which are strongly affected by
the environmental conditions and should be taken into account.
Among
trypanosomatids, T. cruzi has one of the broadest mammal host
ranges, being able to parasitize the most varied tissues, thereby
colonizing almost every niche available. This versatility ensures that
many unorthodox niches such as the opossum scent glands and cartilage
(Deane et al. 1984, Lagrange et al. 1992). This aspect, together with
the capability of maintaining distinct transmission cycles between
sympatric hosts, gives an undoubted advantage to this eclectic parasite
characterizing T. cruzi as one of the most successful organisms
to adopt the parasitic way of life.
REFERENCES