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Importance of wild and synanthropic mammals in public health—Brazil

Since June 2006, Brazil is considered free from Chagas disease transmission due to Triatoma infestans.28 This statement means that the maintenance of a domiciliary Trypanosoma cruzi transmission solely by infected men and domiciliary bugs are not encountered in the country anymore. Human infection nowadays occurs due to vectorial transmission outside the houses, nondomiciliated bugs that invade the houses, or by ingestion of food contaminated with feces of infected bugs.29 In all of these cases, infected wild and synanthropic mammals play a crucial role in the maintenance of parasite circulation.

In a given environment, several mammalian species frequent different forest strata, which favor the parasite exchange among them. Opossums, for example, are habitat generalists and excellent climbers that may be found on the top of trees, although they can also easily be found also on the ground. Opossum species of the genus Didelphis are rather generalist mammals. They can be found dwelling in tree holes and other natural refugees in the forest but they are also highly associated to humans. It is easy to find Didelphis spp. nesting in garbage cans, or even the attic of the houses. Actually, this marsupial genus that is currently considered as a synanthropic animal may act as a very important T. cruzi reservoir and also as a link between the sylvatic and the domestic transmission cycle of T. cruzi.

Several carnivores, such as coatis and weasels, are terrestrial mammalian species that can use tree trunks as refuges. Moreover, coatis construct resting reproduction nests on trees. That means that a given mammal infected through the ingestion of an infected bug on the ground may be later a source of infection for other triatomine species in a hollow tree refuge or in the canopy. In fact, the multiplicity of mammalian host species and possibilities of parasite transmission is probably the main responsible factor for the extremely well-succeeded dissemination of the parasite in the Americas. It is difficult to find a forest fragment in South America where triato- mines and potential mammalian hosts cohabit absolutely free from T. cruzi infection. For this reason, human exposure to the wild environment, during extractive activities for example, common in several areas, but especially in the Amazon basin, should always be considered as a risk of coming into contact with infected triatomines and in acquiring T cruzi infection. Human cases of the disease, as a consequence of this kind of exposure, are very common in the northern part of Brazil (Para State), inside the Brazilian Amazon. These cases occur as outbreaks involving familiar groups and are due to the ingestion of Acai juice contaminated with infected triatomine. , Besides, these outbreaks are clearly seasonal, linked to the Acai” harvest time.33

In nature, T. cruzi transmission cycles assume different profiles that are mostly dependent on the local mammalian fauna, their encounter pattern, and ability to disseminate the parasite, i.e., their infective competence. Since these vary according to parasite DTU and the different conditions of the environment in which they are inserted, it is not possible to predict the intensity of the enzootic cycle before examining the local fauna. Moreover, due to the dynamic character of the T. cruzi transmission network, even surveillance like this, should be considered as restricted to a given period of time. Modifications of local fauna and dynamics of T. cruzi infection may result in higher or lesser prevalence of infection in the local fauna, in a process that is called “amplifier or dilution effect.”34 These kinds of effects were first described for Lyme disease, and since then, applied to other parasitic interactions: Cutaneous Leishmaniasis,35 Hantaviroses,36 West Nile Fever,37 and also Chagas disease.20,38,39

The dilution effect occurs when the number of infected and competent T. cruzi reservoirs (those that display a pattern of infection that favors the parasite transmis- sibility to the vectors) is low when compared to other possible sources of blood meal for triatomines. As a result, the probability of an encounter between one infected and competent reservoir and the triatomine bug is limited, resulting in an overall low prevalence of infection in the local triatomine fauna. Conversely, the amplifier effect is observed when some modification of the environment results in a positive selection of infected mammalian hosts that are competent T. cruzi reservoirs. In this case, the probability of an encounter between infected mammals and triatomine bugs is enhanced, resulting in a higher prevalence of T. cruzi infection in the local triatomine fauna. When such modifications are trigged by men who colonize adjacent forest areas, synanthropic mammalian species—especially marsupials, rodents, and bats—can start to frequent peridomestic areas where they can be a source of a blood meal, i.e., of infection, for triatomines. Hence, environmental modifications imposed by men on areas adjacent to their dwellings, besides all the ecological consequences, could also result in a higher risk of infection by T. cruzi. Infected triatomines are attracted by light and invade the houses where human infection can take place both during the bug’s blood meal or accidentally by the ingestion of food contaminated with feces of infected triatomines. In fact, the latter process seems to be involved in recent outbreaks of Chagas disease in Brazil.20,32

 
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