M. leprae.
Although D. novemcinctus is frequently described as one of the main reservoirs for M. leprae, E. sexcinctus was also described naturally infected for the first time in an endemic area for human Hanseniasis, in Ceará state, northeast of Brazil (Frota et al., 2012). Regardless of the methods applied, M. leprae was not detected in any of the armadillo samples in this study. The results are in accordance with previous studies in the region (Pedrini et al., 2010). Using molecular analysis (PCR) the authors investigated 22 E. sexcinctus , and other three species of armadillo (D. novemcinctus , n = 18; C. unicinctus , n = 2; C. tatouay , n = 2) from two different regions, in the southeast and in the central states of Brazil, including Mato Grosso do Sul state, and all individuals tested negative. According to Truman et al. (2008), negative results might also be related to a non-endemic area for M. leprae , as is the case of the herein investigated areas.
Soil is the probable main habitat for P. brasiliensis. Humans were considered the only hosts of P. brasiliensis for a long time, until the description of naturally infected armadillos in endemic areas of Brazil (Bagagli et al., 2008). Then, the use of molecular analysis enabled the diagnosis of P. brasiliensis in other mammal species, like rodents (Cavia aperea and Sphiggurus spinosus ) and carnivores (Procyon cancrivorus andGallictis vittata ), which are also considered as new hosts for this fungus (Costa et al., 1995; Richini-Pereira et al., 2008; Bagagli and Bosco, 2008).
There is little comprehension about the real meaning of P. brasiliensis infection in armadillos, both for the fungus eco-epidemiology and for the animal health, and its possible impacts in wildlife and conservation. The prevalence of P. brasiliensisinfection in nine-banded armadillos is very high, especially in endemic regions for this parasite where the fungus was isolated in 75-100% of the studied armadillos (Bagagli and Bosco, 2008). Both armadillos andParacoccidioides species have originated and evolved in South America over the last millions of years, with a high likelihood to stablish biological relationships that might be positive for the fungus dissemination while probably neutral for the armadillos. However, we cannot rule out the possibility that this association is actually more recent (e.g. in the last 500 years), as the result of human interference in nature, in a similar manner to the relationship suggested forM. leprae and the nine-banded armadillo (Bagagli et al., 2008; Truman et al., 2011).
As seen for for M. leprae , D. novemcinctus is the most studied species, but P. brasiliensis could also be isolated inCabassous centralis and molecularly detected in D. septemcinctus and D. hybridus (Bagagli and Simões, 2005; Richini-Pereira et al., 2009; Corredor et al., 2005). Although studies performed by several authors presented similar prevalence rates (75-100%; Fernandes et al., 2004; Silva-Vergara et al., 2000; Bagagli et al., 2008; Richini-Pereira et al., 2009), this is the first study describing armadillos infected by P. brasiliensis in a non-endemic area and the species E. sexcinctus infected by this fungus in the Cerrado biome in Mato Grosso do Sul. These results also highlight the importance of the relationship between this fungus and armadillos even in non-endemic areas.
Frequent isolation of P. brasiliensis is usually observed in mesenteric lymph nodes and the fungus has also been molecularly detected in feces samples, suggesting that the armadillo infection might be occurring by alternative routes, like the gastrointestinal tract (Bagagli et al., 2008). Lungs, liver and spleen were the organs whereP. brasiliensis was detected in this study. As described by Bagagli et al. (2008), after the fungus is inhaled by the respiratory tract, the mycelial form can be transformed in yeast in the lungs and be systemically disseminated in armadillos, in a very similar way to that described in humans.
This fungus can survive long periods in the soil, and can also be found inside armadillo burrows (Silva-Vergara et al., 2000; Bagagli and Simões, 2005). The constant digging activity inside burrows may further increase the exposure of armadillos to pathogen inhalation and, based on Silva-Vergara et al. (2000), armadillo infection may increase the long-term viability of the fungus.
5. Conclusion
Armadillo’s ecological studies may also favor the obtaining of relevant information concerning the health status of a given environment. Long-term surveillance health programs involving armadillos should be encouraged, and the data obtained from these should help to better: 1) Understand the prevalence data or occurrence of diverse parasites, especially the zoonotic ones, in the ecosystems they occur; 2) Identify the role of armadillos as reservoir hosts of different parasite species; 3) Provide precise geographic locations and disease risk map analysis; 4) Develop actions and preventive disease control initiatives considering the parasites that can be transmitted by armadillos; and 5) Develop low-cost strategies for health studies considering wild animals, humans and their ecosystems.