Free-ranging wild animal’s species reported positive to
Abstract
The epidemiology of Trypanosoma cruzi in the wild is a particular and highly dynamic scenario that needs attention due to the increased alteration of the environment caused by different factors including anthropogenic change. This chapter is an updated summary about the known reservoir hosts of T. cruzi identified in the countries that share the Amazon rainforest. This information will provide a better understanding of the ecology of T. cruzi in sylvatic environments. This chapter will also contribute to address the potential risks of T. cruzi infection in Amazonian communities who are in contact with wild animals through hunting and wild meat consumption.
Keywords
- Trypanosoma cruzi
- Chagas disease
- Amazon
- parasites
- wild animals
- zoonosis
- host
1. Introduction
The Amazon basin comprises multiple South American countries: Brazil (63.9%), Peru (15.6%), Bolivia (11.7%), Colombia (5.6%), Ecuador (2.1%), Venezuela (0.9%) and Guyana (0.2%). It covers over 1.3 billion hectares with 60% of total forest area (Figure 1) [1]. Population density in the Amazon basin is low and more than 70% live in urban areas. However, this region is in transition due to both climate change as well as anthropogenic activities such as the expansion of agriculture, road paving and logging that lead to accelerated population growth [1, 2].
The environmental conditions of the Amazon basin are favorable for the transmission of multiple vector-borne diseases. Well-known endemic diseases such as malaria and Leishmaniasis show the highest incidence in the Americas, and recent data shows the circulation of multiple arboviruses [3], with an increasing incidence of Dengue fever over time. Trypanosomatids exist in nature since millions of years ago, and Chagas disease has been identified in 4000–9000 year-old human mummies from Chile and Peru [4, 5]. Over time, the spread of Chagas disease in the Americas expanded from a wild and peridomiciliary cycle to a domestic cycle. This occurred through the domiciliation and domestication of triatomines, the primary vectors of
The deforestation of the Amazon basin, 3.6 million hectares of forest lost per year between 2000 and 2010, has become an important factor in the domestication of triatomines due to the scarcity of blood sources among wildlife. Triatomines and other disease vectors have looked for new blood sources and reached areas closer to human dwellings. Social inequality and poor public health systems exacerbate the impact of these factors, especially in rural areas, and further contribute to the transmission of Chagas disease and the emergence of new pathogens.
2. Chagas disease transmission in the Amazon basin
Trypanosomiasis is an ancient enzootic parasitosis in nature, maintained by wild animals and infected vectors. In the wild, it is presumably transmitted primarily by the oral route through predation of infected vectors or mammals, or by contamination of animal nests or shelters with metacyclic forms of the parasite released in the feces of infected triatomines or from scent glands of marsupials i.e.
Besides the wild enzooty, other scenarios for the transmission of
Occupational transmission scenarios are well documented among palm tree gatherers, an economically important activity. Palm trees provide shelter for different wild mammals, amphibians and insects. Gatherers of the piassava palm (
The last scenario is the oral transmission of Chagas disease, often leading to outbreaks of acute Chagas disease (ACD). The Amazon basin is the region where most of such outbreaks have been reported. Actually, Carlos Chagas himself first described ACD in 1909 when a 2-year-old girl from Lassance, Minas Gerais presented with fever, hepatosplenomegaly and Romaña’s sign [8]. ACD outbreaks have occurred in both preserved and human disturbed areas [13], but with exposure of humans to the sylvatic cycle as a common factor. Most ACD outbreaks and cases are related to the consumption of food contaminated with trypomastigote forms as reported with the ingestion of fruits from palm trees such as acaí, bacaba, or the ingestion of wild meat [16]. In fact, ACD cases may have increased in the last decade [16]. It was reported an increase of notified suspected cases in Pará state in Brazil from 2010 to 2016, that may be related to the increase of production to acaí juice during those years, but also related to the increase in its consumption since the majority of patients indicated a daily consumption of this juice [16]. Consistently with these findings, juice contaminated with
In Brazil,
Indigenous communities in the Amazon basin are also affected by
3. Trypanosoma cruzi reservoir hosts in the wild
The first
Order/Genus | Specie | Methods | References | |||
---|---|---|---|---|---|---|
H | I | P | DTU | |||
x | [9] | |||||
x | Zymodeme 1 | [46] | ||||
x | x | TcIV | [9, 28, 46, 47] | |||
x | x | TcI | [9, 48] | |||
x | [9] | |||||
x | x | x | TcI | [9, 46, 47] | ||
x | x | x | TcI, TcII, TcI+ T. rangeli, TcI+ TcII, TcI+ TcIII | [9, 13, 46, 47, 49] | ||
x | x | [49] | ||||
x | [9] | |||||
x | x | x | TcI | [9, 49] | ||
x | x | x | TcI | [9, 13] | ||
x | [47] | |||||
x | [9] | |||||
x | [9] | |||||
x | x | x | TcI | [9] | ||
x | Zymodeme 1 | [46] | ||||
x | x | x | TcI | [9, 13] | ||
x | [9] | |||||
x | Zymodeme 3 | [46] | ||||
x | x | x | TcI, TcI + TcIV | [9] | ||
x | x | x | TcI, TcI+ TcII | [9, 13, 46, 47, 49] | ||
x | x | x | TcI, TcI+ TcIII/TcIV, TcI + T. Rangeli | [9] | ||
x | x | x | TcI+ TcIV | [9] | ||
x | x | x | TcI+ TcIV | [9] | ||
x | [50] | |||||
x | [33] | |||||
x | [33] | |||||
x | [33] | |||||
x | [33] | |||||
x | Zymodeme 1 | [46] | ||||
x | x | TcI, TcI + T.rangeli | [32] | |||
x | [33] | |||||
x | x | [30, 33] | ||||
x | [30] | |||||
x | [50] | |||||
x | [50] | |||||
x | x | x | TcI, TcI + T.rangeli | [9] | ||
x | [33] | |||||
x | x | [28, 47] | ||||
x | x | TcI | [9] | |||
x | [9] | |||||
x | x | x | TcI + T.rangeli | [9] | ||
x | Zymodeme 1 | [46, 47] | ||||
x | [9] | |||||
x | x | [28, 47] | ||||
x | Zymodeme 1 | [46] | ||||
x | [9] | |||||
x | x | x | TcI | [9] | ||
[51] | ||||||
x | [47] | |||||
x | [9] | |||||
x | [9] | |||||
x | [9] | |||||
x | x | x | TcI | [9] | ||
x | x | [9, 47] | ||||
x | x | x | TcI+ TcIII/TcIV | [9] | ||
x | Zymodeme 1 | [46] | ||||
x | Zymodeme 1 | [46] | ||||
x | x | [28, 47] | ||||
[48] | ||||||
x | x | TcI | [9] | |||
x | x | TcI, TcIV | [9] | |||
x | x | TcI | [9] | |||
x | x | TcI | [9] | |||
x | x | TcI | [9] | |||
x | x | TcI | [9] | |||
x | x | TcI | [9] | |||
[52] | ||||||
x | x | TcI | [9] | |||
x | [35] | |||||
x | [35] | |||||
x | x | TcI, TcIV | [9, 52] | |||
x | x | TcI | [9] | |||
x | x | TcI | [9] | |||
[52] | ||||||
[52] | ||||||
[52] | ||||||
[52] | ||||||
[52] | ||||||
x | x | TcI | [9] | |||
x | x | TcIV | [9, 35, 52] | |||
[52] | ||||||
x | x | TcI | [9] | |||
[52] | ||||||
x | x | TcI | [9] | |||
x | x | TcI | [9, 35] | |||
x | x | TcI | [9] | |||
x | x | TcI | [9] |
TcI, TcIII and TcIV are the reported DTUs circulating in the Amazon basin [25]. A very low prevalence of TcIII and TcIV (0.8%) infection was found in 714
The main taxa for the transmission of
3.1 Didelphimorphia
This order includes the hosts most frequently infected by
It is suggested that marsupials could act as generalist species due to the diversity of Trypanosoma spp. found simultaneously infecting a single host [9]. For instance, a mixed, triple infection with
Histopathological lesions observed in infected marsupials resemble those presented by Chagas disease patients. Myocarditis with mononuclear infiltrates, cell lysis and inflammatory infiltrates in skeletal muscles, esophagus and small and large intestines are other lesions found in natural infection [12].
3.2 Carnivores
Carnivores are likely to be infected by the oral route, and those whose diet includes insects or flesh present the highest infection rates [9]. The most reported carnivore infected with
3.3 Non-human primates
Different species of trypanosomatids have been reported in wild non-human primates from the Amazon. The
There is scarce evidence regarding the physiopathology of
3.4 Quiroptera
It was suggested that bats could be bio-accumulator hosts and dispersers of trypanosomatids because of their ability to fly and the great diversity of Trypanosoma species found in bats specially compared to other animal taxon [9]. Out of 1219 Brazilian bats from 76 genera and 94 species, 14% were positive to Trypanosoma sp. by hemoculture and 5% of them were
4. Wild meat consumption as a potential risk of oral transmission
In the Amazon region, wild meat represents an important component of household food security, income and a key social and cultural driver. Wild meat is still a key element in Amazon peoples’ diet and accounts for a high percentage of daily protein intake. It is estimated that the wild meat consumption rate in rural settlements of the Amazon Basin is 172 g per person per day [37]. A study found that 39% of households in Latin America harvested and consumed wild meat, and dependence was highest among the poorest households [38]. Estimates of the annual wild meat harvest in the Northern Peruvian Amazon are 113,000 animals (1680 tons), and 89,224 tons of meat per year in the Brazilian Amazon [39, 40]. Furthermore, hunting pressure has increased in recent years due to various causes, such as the growth of human populations, access to remaining forests, commercialization of wild meat, increasing use of efficient modern hunting techniques and erosion of traditional hunting institutions due to rapid cultural changes [41].
Notwithstanding its positive nutritional contributions, some serious health concerns may be associated with wild meat consumption in the Amazon basin. Emerging infectious diseases worldwide are increasing over time and are dominated by zoonoses (60%), of which the majority (72%) originates in wildlife [42]. A study conducted in the Peruvian Amazon estimated an annually consumption of 45 animals infected with
A few studies from Argentina and Brazil report Chagas disease transmission through consumption of raw, poorly cooked meat, blood or contact with carcasses of wildlife among children [43]. However, some of these studies did not rule out the possibility of vectorial transmission and others have not found proof of exposure to infected triatomines. What it is certainly known is that frequently hunted animals in the Amazon have been reported as
5. Domestic animals as reservoir hosts of Trypanosoma cruzi in the Amazon basin
Domestic animals should be included in epidemiological studies since they are good sentinels of disease transmission in a geographic area. In the Amazon, several studies report
Acknowledgments
This work was supported by the training grant 2D43 TW007393 awarded to Andrés G. Lescano by the Fogarty International Center of the U.S. National Institute of Health, and by ERANet17/HLH-0271.
Conflicts of interest
The authors declare that they have no conflicts of interest regarding the publication of this chapter.
Nomenclature
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