Journal of Vector Borne Diseases

RESEARCH ARTICLE
Year
: 2021  |  Volume : 58  |  Issue : 1  |  Page : 18--27

Ecopathogenic complexes of American trypanosomiasis in endemic areas of Venezuela: Diagnosis and variability of Trypanosoma cruzi


Daisy Lozano-Arias1, Roberto García-Alzate2, Evelyn Tineo3, Mercedes Viettri4, Alexis Mendoza-León5, Cruz M Aguilar6, Antonio Morocoima7, Elizabeth Ferrer4, Leidi Herrera8,  
1 Instituto de Zoología y Ecología Tropical (IZET), Facultad de Ciencias, Universidad Central de Venezuela (UCV), Caracas, Venezuela; Fundación Universitaria Sanmartín. Sede Puerto Colombia. Atlántico-Colombia
2 Instituto de Zoología y Ecología Tropical (IZET), Facultad de Ciencias, Universidad Central de Venezuela (UCV), Caracas, Venezuela; Grupo de investigación en Biodiversidad, Universidad del Atlántico, Barranquilla, Atlántico, Colombia
3 Instituto Pedagógico de Caracas. la Universidad Pedagógica Experimental Libertador (UPEL), Maracay, estado Aragua, Venezuela
4 Instituto de Investigaciones Biomédicas “Dr. Francisco J. Triana Alonso” (BIOMED), Universidad de Carabobo Sede Aragua, Maracay, estado Aragua, Venezuela
5 Facultad de Ciencias, Instituto de Biología Experimental (IBE), Universidad Central de Venezuela, Caracas, Venezuela
6 Centro de Investigaciones en Enfermedades Tropicales (CIET-UC), Facultad de Ciencias de la Salud, Universidad de Carabobo, San Carlos, Cojedes, Venezuela
7 Centro de Medicina Tropical de Oriente, Universidad de Oriente (UDO) Núcleo Anzoátegui, Barcelona, estado Anzoátegui, Venezuela
8 Instituto de Zoología y Ecología Tropical (IZET), Facultad de Ciencias, Universidad Central de Venezuela (UCV), Caracas, Venezuela

Correspondence Address:
Leidi Herrera
Instituto de Zoología y Ecología Tropical (IZET), Facultad de Ciencias, Universidad Central de Venezuela (UCV), Caracas
Venezuela

Abstract

Background & objectives: Trypanosoma cruzi, the causative agent of American trypanosomiasis, has been reported in 180 mammalian species and 154 triatomines species of Neotropic. This is a clonal parasite with variable biological behaviour, associated with the genetics of the parasite and its hosts. To know the eco-pathogenic complex of this zoonosis, it was proposed to characterize T. cruzi isolates obtained from triatomines and domestic, peridomestic and wild mammals of the eastern and central-western regions of Venezuela. Methods: The positivity to T. cruzi was established and the isolates were genetically characterized by PCR amplification of the mini-exon gene, the DNA coding for 24Sa and 18S rRNA, and polymorphic sequences-RFLPs. The sampling sites were georeferenced using the MapSource Software and ArcGis 9.3 programs to generate distribution maps of the isolates. Results: Of the 460 hosts (205 triatomines and 255 mammals), 49% were positive for the parasite. On the other hand, 38 isolates obtained from the triatomines and 23 isolates obtained from mammals were evaluated. The TcI genotype predominated in most of the isolates; however, in those obtained from triatomines the presence of the TcIII genotype in single infections and TcI + TcIII or TcI + TcIV in mixed infections was also evidenced. Interpretation & conclusion: There is a possibility that the triatomines act as biological syringes for these genotypes associated exclusively to them. The heterogeneity in T. cruzi isolates demonstrated the complexity of parasitosis in these regions, presenting its control and prevention as a challenge.



How to cite this article:
Lozano-Arias D, García-Alzate R, Tineo E, Viettri M, Mendoza-León A, Aguilar CM, Morocoima A, Ferrer E, Herrera L. Ecopathogenic complexes of American trypanosomiasis in endemic areas of Venezuela: Diagnosis and variability of Trypanosoma cruzi.J Vector Borne Dis 2021;58:18-27


How to cite this URL:
Lozano-Arias D, García-Alzate R, Tineo E, Viettri M, Mendoza-León A, Aguilar CM, Morocoima A, Ferrer E, Herrera L. Ecopathogenic complexes of American trypanosomiasis in endemic areas of Venezuela: Diagnosis and variability of Trypanosoma cruzi. J Vector Borne Dis [serial online] 2021 [cited 2021 Nov 27 ];58:18-27
Available from: https://www.jvbd.org/text.asp?2021/58/1/18/321749


Full Text

 Introduction



Trypanosoma cruzi (Eucarya, Kinetoplastea, Tripanosomatidae), the causative agent of the American trypanosomosis (AT) or Chagas disease (Chd), is a clonal hemoflagellate, with genetically defined subpopulations, that constitute a biocoenosis, geographically framed in the existence of wild and domestic mammals of up to 10 orders that act as hosts, and strict hematophagous insects, the triatomines, which act as biological vectors. T. cruzi is grouped into Discrete Typing Unit (DTUs) which reflect the diversity associated with domestic and wild domestic transmission cycles in a process of parasite selection as it passes through different species of triatomines and mammals including human[1],[2].

The AT or Chd as a zoonosis had been considered, until recently exclusive of the Neotropics, affecting 7 million people, mostly circumscribed to the rural habitat[3]. Frequently, it is reported in the United States, Canada, Europe, Japan and Australia, due to the progressive increase of human migrations. In all cases, the use of land, agricultural practices and the indiscriminate handling of animals are linked, affecting environmentally on small and large scale. With the domiciliation of the triatomines and the synanthropic behavior of mammals, the passage of enzootia to the zoonosis has been favored, which increases the exposure to the parasite, as evidenced by the presence of T. cruzi in several species of wild hosts, pets and synanthropic or hunting fauna[4],[5].

There are few research studies which overlap the diagnosis of T. cruzi, its genotypic variability and the presence of elements of the natural history of parasitism in its niches. In the present work the study of elements of the ecopathogenic complex were proposed. The study of peri-domiciliary and domiciliary endemic areas to the TA or Chd in states of the west, center and the eastern regions of Venezuela, allowed to know the potential geographical expansion of the zoonosis, by analysis of the presence of vectors, reservoirs, distribution of genotypes, performing potential ecological niche models and providing data for monitoring and epidemiological control[6],[7],[8].

 Material & Methods



Study areas

The study was conducted in communities in the central-western region of Venezuela, (Cojedes, Portuguesa, Miranda states and Capital District) and eastern states (Anzoátegui and Sucre states) [Table 1] whose inclusion criteria were the previous records of the presence of the parasite, presence of infected mammals including human and/or presence of T. cruzi positive triatomines[6],[8],[9],[10]. We reviewed domestic, peridomestic and wild ecotopes as a continuum of peri domiciliary area for the search of mammals and triatomines presence. The study areas were georeferenced through a global positioning system Garmim III GPS (Garmin International, Olathe, KS) using the programs Map Source Software and ArcGis 9.3 (Environmental Systems Research Institute, Redlands, CA, USA) and its biome described according to the life tables of Venezuela[11] [Table 1].{Table 1}

Sampling of triatomines and mammals

A non-probabilistic sampling was carried out, in representative areas with no less than 20 host records (mammals and/or triatomines) in which the presence of T. cruzi had been detected in vectors, reservoirs and/or a human population, with zero as presence or absence value[10],[12],[13].

Triatomines

Triatomines were collected manually during visits in the day and evening in human dwellings (D = domestic), up to 20 m in diameter from the outermost part of the dwelling (PD = peridomestic) and in an area towards a wild corridor (WC), beyond 30 m from the PD and to the nearby fields (1000 m) that surrounded the localities. The vegetation, furnishings, bird nests, caves, poultry houses and stables were reviewed using 1 hour/man/dwelling, with three operators for three sampling days per region. The samplings were carried out twice a year in each region, taking care to cover periods of rain and drought[14],[15].

An active search for triatomines was achieved by training the inhabitants for the recognition of triatomines and their safe collection, when they approached homes attracted by light. The triatomines were registered according to place of collection, time and sex, geo-referenced and maintained for review and identification according to Lent and Wygodzinsky[16].

Mammals

In the D, PD and WC, mammals were captured, using “National” traps (Tomahawk livetraps Co. Tomahawk, Wisconsin, USA, Mod.201 -40.6×12.7×12.7 cm; Mod 204-50.8x17.9x17.9 cm) and traps “Sherman” (Tomahawk livetraps Co; Mod 101 -25.4×7.6×7.6 cm) separated each by 10 m and placed between 6 pm and 6 am. The traps were baited with universal bait. Mammal sampling was carried out twice a year in each region at a rate of 3 days per visit to the house and 4 hours/man/night effort for each day of the capture, in rain and drought period”. Mammals were identified according to Sánchez and Lew[17]. The captured mammals were sedated with intramuscular Ketamine® at a rate of 10 mg/kg for blood sampling by cardiac puncture and sterile blood culture on NNN diphasic blood agar (Novy, Nicolle and McNeal) to search for trypanosomatids, by interdiary review of cultures, for up to six months after inoculum. Additionally, a xenodiagnosis was performed, with 10 to 20 individuals of R. prolixus (triatomines) of III or IV nymphal stage, proven healthy and reared in the laboratory to obtain flagellates compatible with blood Trypanosoma morphotypes[18].

Parasitological diagnosis

The feces and digestive tract of collected triatomines were checked, in sterile isotonic solution (0.85%) under a microscope (400X) for the search of flagellates compatible with T. cruzi morphotypes. This procedure was also performed on experimental xenodiagnosis triatomines used on mammals, from 7 days post intake and for up to 6 months. The hemolymph and salivary glands were examined under a microscope to search for Trypanosoma rangeli[19]. The metacyclic trypomastigotes of the fecal samples/ salivary glands of triatomines were inoculated via i.p., at a rate of 200 metacyclics/g of weight in male Mus musculus NMRI of 10 g. The recovery of the isolates and closure of the cycle was carried out by means of xenodiagnosis on the animals with the highest parasitaemia, for subsequent extraction of 0.5 mL of blood for NNN culture[18].

Molecular diagnosis and variability of T. cruzi isolates

Stool samples of triatomines or material of NNN culture were subjected to DNA extraction by Wizard Genomic® kit (Promega). The purity was calculated by the A260/280nm ratio and the integrity was corroborated by electrophoresis in 0.8% agarose gel at 80V, in TAE buffer (0.04 M Trisma Acetic acid, 0.001 M EDTA) stained with Ethidium Bromide and visualized in Gel Doc 1000 (Bio-Rad). The molecular diagnosis of T. cruzi was made by amplification of the kDNA sequence, based on the polymerase chain reaction (PCR)[20]. The genetic variability of T. cruzi isolates was studied by using molecular markers: (i) intergenic region of the miniexon, (ii) D7 divergent domain of the 24Sa rDNA and (iii) size-variable domain of the 18S rDNA. PCR-RFLP of HSP60, GPI and H1 was performed[21],[22]. The products were evidenced by electrophoresis in agarose gels (Agarose Ultra pure Sigma®) at 2% using TAE (40 mM Tris Acetate Buffer, 0.5 M EDTA pH 8.0) under running conditions of 80-100V. The DNA bands stained with ethidium bromide were visualized with UV using the Gel Doc 1000 system (BioRad). The size of the products of the PCRs was estimated by comparing the band pattern of the molecular size marker 100 bp (Promega®) or 100 bp Hypperladder IV (Axygen®) [Table 2].{Table 2}

Modelling of the actual and potential niche of T. cruzi isolated from mammals and triatomines

The T. cruzi distribution map was generated with geo-referenced records of parasite presence in mammals and triatomines, associated with 19 climatic variables and a spatial resolution of a 1 Km2 pixel in Ecuador, resulting from the interpolation of mean temperature data, monthly precipitation and altitude data climatic (interpolation of average monthly climatic data from meteorological stations over 30-50 years - WorldClim project)[23].

Using the MAXENT software, a run of ten models was performed to generate a model of average values using 1000 iterations, a convergence threshold of 1.0 × 10-5, with 75% of the records for the calibration of the model and 25% for its evaluation (Maximum Entropy model). The output of the MAXENT model was converted by DIVA GIS software, resulting in the map with a cut-off threshold of the 10th percentile. The percentage contribution of each variable and the Jackknife test allowed to know the importance of each variable, alone or as a whole, on the potential distribution of the parasite in their hosts[24],[25].

Ethics statement

All applicable international, national, and/or institutional guidelines were followed. The study was approved by the Ethics Committee of the Instituto de Biomedicina de la Universidad de Carabobo, under the number CBIIB (UC) 2012-2, which endorsed the Project 2007001442 Science Mission-MPPCTI, which has been supporting part of the research carried out.

 Results



Triatomines

We obtained 205 triatomines of which 133 (65%) were collected in the eastern region and 72 (35%) in the western region. The species in order of predominance in the eastern region were T. maculata, P. geniculates, R. prolixus, R. picitipes, Ps. arthuri, E. cuspidatus, observing greater variability in terms of triatomine species sampled in relation to the central-western region in which only three species were collected, which in order of predominance were P. geniculatus, R. prolixus and T. maculata.

The prevalence of positive triatomines to T. cruzi, parasites in faeces and PCR (presence of a 330 bp band for the amplification of kDNA), was 62% (82/133 triatomines) discriminated by species of higher prevalence of infection such as T. maculata, P. geniculatus, R. prolixus, Ps. arthuri, R. pictipes and E. cuspidatus for the eastern region. The prevalence of positive triatomines to T. cruzi was 71% (51/72 triatomines), discriminated by species with greater prevalence of the parasite such as P. geniculatus and R. prolixus, for the central-western region. Of the totality of positive triatomines for T. cruzi, 28.4% was used for its culture and genotypic characterization.

Mammals

255 specimens of 16 species of the Venezuelan mastofauna were obtained, of which 83 (32%) were found in the eastern region and 172 (67%) in the central-western region. The species for the eastern region were varied, with domestic, synanthropic and wildlife exemplars, representing 32% of the studied mammals. The species in decreasing predominance were: Canis familiaris, Didelphis marsupialis, Equus asinus, Rattus rattus, Bos taurus, Equus asinus x Equus caballus, Equus caballus, Riphidomys couesi, Cerdocyon thous, Cuniculus paca, Dasypus novencinctus, Desmodus rotundus, Odocoileus margaritae, Odocoileus virginianus, Sus scrofa and Tamandua tetradactyla. The species of mammals collected in the central-eastern region, were essentially domestic or synanthropic, representing 30% of the mammals studied with a predominance in decreasing order for C. familiaris, D. marsupialis, Equus asinus, R. rattus and Equus aisnus x Equus caballus.

The positivity of these mammals to T. cruzi, eliminate established by parasitological (hemoculture/xenodiagnostic) and/or molecular methods (amplification of kDNA) was 43.4% (36/83 mammals) in the eastern region, discriminated from higher to lower prevalence eliminate of infection: D. marsupialis, C. familiaris, Equus asinus, Bos taurus, R. rattus, Cerdocyon thous, Odocoileus margaritae and Tamandua tetradactyla. The T. cruzi positivity of mammals was 30% (51/172 mammals) in the central-western region, discriminated from higher to lower prevalence : Canis familiaris, D. marsupialis, Equus asinus, Equus aisnus x Equus caballus, R. rattus.

Study of genetic variability

The genetic variability pattern of T. cruzi subpopulations observed by the ME, 24Sa, 18S markers and RFLPs, for 38 triatomine isolates, revealed that for the eastern region, 72% (10/14) amplified for TcI and 21% (3/14) for TcIII (2 isolates obtained from P. geniculates and 1 from Ps. arthuri). The remaining 7% (1/14, obtained from T. maculata) showed a mixed infection TcI/ TcIII and RFLP pattern compatible with TcV. Of the 24 T. cruzi isolates from triatomines from the central-western region, 96% (23/24) amplified for TcI and 4% (1/24) revealed a mixed infection TcI/TcIV in one specimen of R. prolixus enlightening genetic heterogeneity in these triatomine isolates [Table 2] & [Figure 1],[Figure 2],[Figure 3],[Figure 4].{Figure 1}{Figure 2}{Figure 3}{Figure 4}

Analysis using ME, 24Sα, 18S markers and RFLPs from the 23 T. cruzi isolates obtained from mammals in the eastern and central-western regions of Venezuela, confirmed homogeneity with respect to the DTU of the parasite, all exclusively TcI [Table 2] & [Figure 1] [Figure 3], [Figure 5].{Figure 5}

Potential geographic distribution of the elements of the zoonoses

The predictive model generated by Diva GIS and MAXENT with the geolocalized positives mammals and triatomines in the present study, produced a map of potential distribution of T. cruzi with occurrence, based on T. cruzi presence data in mammals and/or triatomines associated with preponderating bioclimatic characteristics. The highlighted areas indicated that there was a 0.556-1 probability of finding the T. cruzi parasite in mammals and/or insects, in focal areas of the coastal mountain range such as Sucre, Monagas and Anzoátegui states (of the Eastern region) and Miranda, Aragua, Lara, Falcón, and Zulia (from the central-western region). In an exceptional way, the model predicted with the same probability the presence of T. cruzi in mammals and/or insects, in focal areas of Merida State.

The variables of those regions that would seem to have contributed more in percentage for the potential establishment of the zoonosis were: precipitation of the driest month (23.8%), precipitation of the coldest quarter (23.7%) and average temperature of the warmest quarter (10%). The six variables of minor contribution were: Annual Precipitation (7.9%); Isothermality (7 %); Seasonality of the temperature (5.8%), Precipitation of the wettest quarter (5.4%), Precipitation of the wettest month (4%); Altitude (3.6%), Average daytime temperature range (Temperature, Maximum-Temperature Minimum, 2.9%) and Average temperature of the wettest quarter (2.7%). The bioclimatic variable that by itself predicted the potential establishment of a niche of the zoonosis with the highest contribution values in data distribution (Jackknife AUC test) was the annual precipitation, which gave more useful information when analyzed in isolation. An area under the curve (AUC) of 0.94, gave effectiveness to the model of potential T. cruzi distribution in the study regions [Figure 6].{Figure 6}

 Discussion



The AT or Chd, is a complex parasitosis that manifests from an enzootia to an anthroponosis, depending on the trophic network in which it is circumscribed and in which several species of triatomines and mammals can participate, including the human. Recently, it has been considered a re-emerging parasitic disease conditioned by anthropogenic changes in wild and urban habitats[3],[26],[27],[28].

The TA in Venezuela has traditionally been associated with the foot of the Andean mountain, the Central-Eastern mountain range and the elevations of the central-western plains, areas of greater distribution of human settlements[29]. Recent studies have revealed an increase in incidence in coastal areas and other regions of eastern and southern Venezuela, such as Anzoátegui, Nueva Esparta and Amazonia[9],[30],[31].

The vectors in the transmission cycle

In Venezuela, 60% of the confirmed cases of Chd have been reported in Anzoátegui, Aragua, Barinas, Carabobo, Cojedes, Portuguesa, Trujillo and Yaracuy, the majority of these being associated with the presence of R. prolixus domiciliary primary vector[6],[8],[10],[30]. This scenario has changed in the central-western region of Venezuela, due to the occasional visit or colonization in human habitation by T. maculata and P. geniculatus, both attracted by artificial light from nearby wild niches, or by the decrease of mammals, their source of food, due to human anthropized habitats or subsistence hunting activities[30],[32],[33],[34].

The results presented here, although they are a specific entry, revealed diversity of the triatominofauna, with a preponderant presence of P. geniculatus, followed by T. maculata and R. prolixus species with relevant epidemiological roles in Venezuela and with the potential of domiciliation, evidenced in the eventual existence of nymphal stages in human settlements. Other species found, would be acting as occasional vectors such as Ps. arthuri, E. cuspidatus and R. pictipes, all subject of mandatory epidemiological surveillance in the domestic, peridomestic and wild transmission cycle[6],[13],[15],[35],[36],[37],[38],[39].

In particular, Ps. arthuri reported in Anzoátegui, Cojedes and Portuguesa with natural infection by T. cruzi, could be considered a cryptic vector, increasing in peri-domestic ecotopes, specifically in bird nests, less than five meters from human habitation and in sympatry with other triatomines and some mammals. These potential vectors could, at any time migrate to homes and be in contact with humans and peridomestic or domestic animals, constituting a risk factor[39].

The genotype of T. cruzi that appeared mostly in P. geniculatus, T. maculata and R prolixus was TcI, originally associated with wild cycles, however, it has recently been syndicated to domestic transmission cycles that go from Central America to the Amazon basin (north of South America)[2]. The species E. cuspidatus, associated mainly with domestic and peridomestic ecotopes, has been found infected with TcI in the present work. The reports of infection in the literature only refer to E. mucronatus, species of more recent speciation, infected with TcI. Thus, this would be a new finding of consideration in the distribution of this T. cruzi genotype[13],[38].

R. pictipes, registered in association with wild cycles for T. cruzi and T. rangeli in palms, bromeliads, caves of mammals and dry trees, was found in peridomestic ecotopes, with 100% positivity for TcI, indicating its high degree of adaptation to anthropized environments as cited in literature[38]. In the present work, TcIII was found in unique infections in P. geniculatus and Ps. arthuri, The distribution of TcIII, has been increasing in the country, acquiring epidemiological importance, insofar as it has been considered a bioindicator of the existence of biological corridors between the cycles of wild and peridomestic transmission and particularly associated with the armadillos as reservoirs[2],[6],[29],[39],[40].

Some theories, indicate that the parasite-vector association is much older than that of the parasite-mammal, since the insects were primarily predators with secondary incorporation of the hematophagy[41], favoring their action as true “biological syringes” that spread more than one parasite genotype, this could explain the genetic variability that is revealed in mixed infections with the TcI + TcIV and TcI + TcIII, genotypes, observed in T. maculata and R. prolixus respectively.

The mammal in the transmission cycle

In the present work several species of mammals were studied, acting as potential reservoirs for T. cruzi, all infected with TcI, with the ability to interact with triatomine vectors mentioned above and in areas where an infected human population has been registered, being able to form ecopathogenic complexes[1],[6],[26],[37],[42],[43]. In this study D. marsupialis was the species, with the highest prevalence, 50% exclusively TcI, that has been considered in some ecosystems a primary synanthropic reservoir, with wide geographic distribution, omnivorous habits, and eclectic niches, such as the corridors between wild and domestic environments. It is characterized by high rates of infection and can eliminate infectious forms in the urine and the content of their anal glands, eventually contaminating food and home equipments, which constitutes a high risk[27],[44],[45].

Other wild mammals, components of the Venezuelan hunting fauna, were positive, such as T. tetradactyla, O. margaritae, D. novencintus, P. tajacu, C. paca, C. thous, which have been reported as infected with T. cruzi in the country and in other areas of America. These species could act as reservoirs and dispersers, especially when participate in the human food chain; it is necessary to establish their population dynamics within the transmission cycle[1],[33]. It should be noted that the infection in chiroptera specimens such as D. rotundus and in foxes such as C. thous is the first record, being that the results obtained here constitute a contribution to the data reservoirs in Venezuela.

The positivity to T. cruzi of animals used for livestock such as equidae, is also a finding of great epidemiological importance since in critical situations in agricultural practice, humans concentrate the population of these animals in areas, for saving food, water and labour for management, leading to overcrowding. This aggregation would facilitate the attraction of vectors, forcing a bottleneck, and creating a greater risk of transmissibility, in artificially favoured transmission cycles. The possibility of transmission of T. cruzi in humans involved in livestock management, their families, or in a livestock-marketing route, by handling raw meat and/or consuming under-cooked meat with circulating blood stages of the parasite it is something that could not be ruled out[46],[47].

In the exposed results, the positivity to T. cruzi in dogs constitutes an important contribution to the few studies about the role of the dog in the transmission cycle, in Venezuela. The dog would be considered in surveillance programs, for its role as a sentinel of the AT in areas with re-emergence, post chemical vector control or post human treatment. In non-endemic areas, it could act as an indicator of the emergence of the zoonosis[30],[42],[46],[48],[49],[50]. In our study, the isolates of T. cruzi obtained from D. marsupialis, cinegentic mastofauna and synanthropic and domestic fauna, revealed long periods of infection with continuous parasitic load, low parasitemia values and variable mortality rate in a murine model. This would guarantee continuous transmissibility, independent of the geographical area (data not shown).

State of art

T. cruzi is a complex of heterogeneous subpopulations, over artificial and natural stress as the uncontrolled extension of the cities towards forests and savannas, deforestation, migration of the hosts (including humans) from wild/ rural landscapes to suburban and urban habitats, leading to selection of parasite subpopulations.

In our study, this heterogeneity was reflected in the higher prevalence of TcI, followed by the TcIII genotype prevalence and a little representation of mixed genotypes TcI + TcIII and TcI + TcIV (TcV?). The presence of the TcI genotype in the three ecotopes would indicate its transmission among the hosts independent of the ecotope, breaking the classical conception of associating a genotype with a specific transmission cycle[2].

Likewise, the eclectic range of mammals and triatomines species associated with TcI (E. cuspidatus, R. pictipes, O. margaritae, D. rotundus, P. tajacu and C. thous) would explain why the ample TcI dispersion in the country, conditioned by hosts niches that favour host-parasite encounter and determine the host role in the transmission cycles[6],[26],[37],[43],[50].

The parasite-host relationship is part of a larger system, represented by communities and ecosystems in which all the elements of the association are present, especially when its distribution coincides with major human settlement distributions in Venezuela. The phenomenon of emerging, neglected or re-merging diseases would be understood since the complex paradigm. These maladies involve ecological and evolutionary mechanisms that participate in the passage from wild to domestic environments and vice versa[51].

The studies of parasite reservoirs are important for control and epidemiological surveillance. The risk would imply the presence of these hosts in peridomestic and domestic ecotopes, associated with hunting and consumption of wild animals. Likewise, know the T. cruzi prevalence in cinegetic wild fauna, favours the early detection of a wide range of zoonosis. However, with a punctual entry is difficult to define exactly the role of some mammal species; longitudinal studies are more representative to clarify this eco-pathogenic complex[1],[26].

Research on TA in Venezuela has been focused on the clinical and epidemiological behaviour; occasionally some researchers have analysed the biological tendencies of the parasitosis, but not as a whole. This study contributes to discern to some aspects of the real or potential eco-pathogenic complex and provides elements for the modelling of T. cruzi distribution.

Conflict of interest: None

 Acknowledgements



This investigation received financial support from Proyecto Misión Ciencia N° 2008000911-6, FONACIT, MPPS, Proyecto Estratégico UCV-UC-UDO, FONACIT, MPPS, N° 2011000470 Proyecto en Red. Subproyecto No 2007001442. Misión Ciencia MPPCT-Venezuela.

References

1Herrera L. Una revisión sobre reservorios de Trypanosoma (Schizotrypanum) cruzi (Chagas, 1909), agente etiológico de la Enfermedad de Chagas. Bol Mal Salud Amb 2010; 50: 3–15.
2Zingales B, Miles MA, Campbell DA, Tibayrenc M, Macedo AM, Teixeira MMG, et al. The revised Trypanosoma cruzi sub-specific nomenclature: Rationale, epidemiological relevance and research applications. Infect Genet Evol 2012; 12(2): 240–53
3World Health Organization 2019. Chagas Disease (American trypanosomiasis). Fact sheet. Available from: https://www.who. int/en/news-room/fact-sheets/detail/chagas-disease (Accessed on April 17, 2019).
4Colwell DD, Dantas-Torres F, Otranto D. Vector-borne parasitic zoonoses: Emerging scenarios andnew perspectives. Vet Parasitol 2011; 182(1): 14–21.
5Viettri M, Herrera L, Aguilar CM, Morocoima A, Reyes J, Lares M, et al. Molecular diagnosis of Trypanosoma cruzi/Leishmania spp. coinfection in domestic, peridomestic and wild mammals of Venezuelan co-endemic areas. Vet Parasitol Reg Stud Reports 2018; 14: 123–130.
6Carrasco H, Segovia M, Llewellyn M, Morocoima A, Urdaneta-Morales S, Martínez C, et al. Geographical distribution of Trypanosoma cruzi genotypes in Venezuela. PLoS Negl Trop Dis 2012; 6(6): e1707.
7Urdaneta-Morales S. Chagas’ disease: an emergent urban zoonosis. The Caracas Valley (Venezuela) as an epidemiological model. Front Public Health 2014; 2(265): 1–13.
8Morocoima A, Barroeta R, Virguez M, Roschman-González A, Chique JD, Ferrer E et al. Infección natural por Trypanosoma cruzi en triatominos que habitan en la Palma Corozo (Acrocomia aculeata) en regiones del oriente de Venezuela. Rev Peru Med Exp. Salud Pública 2018; 35(4): 563–72.
9Morocoima A, Tineo E, Ferrer E, Herrera L, Nuñez M. Enfermedad de Chagas en el estado Anzoátegui, Venezuela: Registro de un caso agudo y caracterización parasitológica y molecular del aislado. Bol Malariol Sal Amb 2008; 48 (2): 121–126.
10Morocoima A, Chique J, Zavala-Jaspe R, Díaz-Bello Z, Ferrer E, Urdaneta-Morales S, et al. Commercial coconut palm as an ecotope of Chagas disease vectors in northeastern Venezuela. J Vector Borne Dis 2010; 47(2): 76–84.
11Ewel J.J, Madriz A, Tosi J. Zonas de vida de Venezuela. Memoria explicativa sobre el mapa ecológico 1976; 2nd edition. Ministerio de Agricultura y Cría, Fondo Nacional de Investigaciones Agropecuarias. Caracas. 265 pp.
12Non-Probability Sampling. 2009. Available from: http://explorable.com/non-probability-sampling.html (Accessed on June 24, 2013).
13Morocoima A, Chique J, Herrera L, Urdaneta-Morales S. Eratyrus mucronatus (Stal, 1859) (Hemiptera, Reduviidae, Triatominae): primer registro para el estado Anzoátegui (Venezuela). Bol Malariol Sal Amb 2010; 48(2): 307–310.
14Bautista NL, García de la Torre GS, De Haro I, Salazar-Shettino PM. Importance of Triatoma pallidipennis (Hemiptera: Reduviidae) as a vector of Trypanosoma cruzi (Kinetoplastida: Trypanosomatidae) in the state of Morelos, México and possible ecotopes. J Med Entomol 1999; 36(3): 233–5.
15Reyes-Lugo M. Panstrongylus geniculatus Latreille 1811 (Hemiptera: Reduviidae: Triatominae), vector de la enfermedad de Chagas en el ambiente domiciliario del centro-norte de Venezuela. Rev Biomed 2009; 20: 180–205.
16Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas disease. Bull. Amer Mus Nat Hist 1979; 163: 123–520.
17Sánchez J, Lew. Listado de los Mamíferos de Venezuela. Mem Fund La Salle Ciens Nat 2010; 173–238.
18Herrera L, Morocoima A, Aguilar C.M, Urdaneta-Morales S. Trypanosoma cruzi: parasitismo del tejido conectivo adiposo. Rev Cient FCV-LUZ 2005; 15(3): 210–216.
19D’ Alessandro A, Saravia N. Trypanosoma rangeli. In: Lumsden WHR, Evans DA. editors, Parasitic Protozoa. Academic Press 1992; 1–54.
20Wincker P, Britto C, Pereira JB, Cardoso MA, Oelemann W, Morel CM. Use of a simplified polymerase chain reaction procedure to detect Trypanosoma cruzi in blood samples from chronic chagasic patients in a rural endemic area. Am J Trop Med Hyg 1994; 51(6): 771–777.
21Brisse S, Verhoef J, Tibayrenc M. Characterisation of large and small subunit rRNA and mini-exon genes further supports the distinction of six Trypanosoma cruzi lineages. Int J Parasitol 2001; 31(11): 1218–1226.
22Lewis MD, Ma J, Yeo M, Carrasco HJ, Llewellyn MS, Miles MA. Genotyping of Trypanosoma cruzi: systematic selection of assays allowing rapid and accurate discrimination of all known lineages. Am J Trop Med Hyg 2009; 81(6): 1041–1049.
23Fick SE, Hijmans R.J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol 2017; 37(2): 4302–4315.
24Phillips SJ, Anderson RP, Schapireet RE. Maximum entropy modeling of species geographic distributions. Ecol. Model 2006; 190(3-4): 231–259.
25Haverkost TR, Gardner SL, Peterson AT. Predicting the distribution of a parasite using the ecological niche model, GARP. Rev Mex Biodivers 2010; 81(3): 895–902.
26Herrera L. Trypanosoma cruzi, the causal agent of Chagas disease: boundaries between wild and domestic cycles in Venezuela. Front Public Health 2014; 2: 1–4.
27Díaz-Bello Z, Zavala-Jaspe R, Reyes-Lugo M, Colmenares C, Noya-Alarcón O, Noya O, et al. Urban Trypanosoma cruzi Oral Transmission: from a Zoonotic Founder Focus to the Largest Microepidemic of Chagas Disease. SOJ Microbiol Infect Dis 2016; 4: 1–9.
28Rivera IM, Moreno EA, González N, Lugo A. Caracterización de aislados de Trypanosoma cruzi del occidente de Venezuela. Rev Ecol Latin Amer 2000; 7: 1–10.
29Morocoima A, Carrasco HJ, Boadas J, Chique JD, Herrera L, Urdaneta-Morales S. Trypanosoma cruzi III from armadillos (Dasypus novemcinctus novemcinctus) from Northeastern Venezuela and its biological behavior in murine model. Risk of emergency of Chagas’ disease. Exp Parasitol 2012; 132(3): 341–7.
30Berrizbeitia M, Concepción JL, Carzola V, Rodriguez J, Cáceres A, Quiñones W. Seroprevalencia de la infección por Trypanosoma cruzi en Canis familiaris del estado Sucre, Venezuela. Biomédica 2013; 33(2): 214–25
31Noya-Alarcón O, Botto C, Cortez J, Ferrer E, Viettri M, Herrera L. Primer registro de Panstrongylus geniculatus (Latreille, 1811) en los municipios Alto Orinoco y Atures, estado Amazonas, Venezuela. Bol Mal Salud Amb. 2011; 51(1): 81–85.
32Reyes-Lugo M, Reyes-Contreras M, Salvi I, Gelves W, Avilán A, Llavaneras D, et al. The association of Triatoma maculata (Ericsson 1848) with the gecko Thecadactylus rapicauda (Houttuyn 1782) (Reptilia: Squamata: Gekkonidae): A strategy of domiciliation of the Chagas disease peridomestic vector in Venezuela? Asian Pac J Trop Biomed 2011; 1(4): 279–284.
33Morocoima A, Cifuentes-Larez AE, Delgado-Díaz MJ, Urdaneta-Morales S. Mamíferos cinegéticos de Venezuela: riesgos epidemiológicos en la infección con Trypanosoma (Schizotrypanum) cruzi. Rev Cien, FCV-LUZ 2018, XXVIII: 32 – 41.
34Morocoima A, De Sousa L, Herrera L, Roja SL, Villalobos M, Chique J, et al. Simpatría de triatominos (Reduviidae) y escorpiones (Buthidae) en Coccus nucifera y Acrocomia aculeata (Aracaceae) de Anzoátegui, Venezuela. Bol Mal Salud Amb. 2011; 51(2): 187–198
35Cermeño JW. Infección por Trypanosoma cruzi en el estado Bolívar, Venezuela. revisión y actualización. Saber 2013; 25: 129–141.
36García-Jordan N, Berrzbeitia M, Concepción JL, Aldana E, Caceres A, Quiñones W. Estudio entomológico de vectores transmisores de la infección por Trypanosoma cruzi en la población rural del estado Sucre, Venezuela. Biomédica 2015; 35: 247–57.
37Añez N, Crisante G, Añez-Rojas N, Rojas A, Moreno G, Da Silva F, et al. Genetic typing of Trypanosoma cruzi isolates from different hosts and geographical areas of western Venezuela. Bol Mal Salud Amb 2009; 49(2): 251–258.
38Cazorla-Perfetti DJ, Nieves-Blanco EE. Triatominos de Venezuela: aspectos taxonómicos, biológicos, distribución geográfica e importancia médica. Avances cardiol 2010; 30(4): 347–369.
39Cruz-Guzmán PJ, Morocoima A, Chique JD, Ramonis-Quintero J, Uzcátegui M, Carrasco H. Psammolestes arthuri naturalmente infectado con Trypanosoma cruzi encontrado en simpatría con Rhodnius prolixus y Triatoma maculata en nidos de aves en el estado Anzoátegui, Venezuela. Saber 2014; 26: 428–440.
40Martins K, Andrade C, Barbosa-Silva AN, do Nascimineto GB, Chiari E, Galvao LM et al. Trypanosoma cruzi III causing the indeterminate form of Chagas disease in a semi-arid region of Brazil. International Journal of Infectious Diseases 2015; 39: 68–75.
41Gaunt MW, Miles MA. The ecotopes and evolution of triatomine bugs (Triatominae) and their associated trypanosomes. Mem Inst Oswaldo Cruz 2000; 95(4): 557–565.
42Crisante G, Rojas A, Teixeira M, Añez N. Infected dogs as a risk factor in the transmission of human Trypanosoma cruzi infection in western Venezuela. Acta Trop 2006; 98(3): 247–254.
43Rivera MG, Herrera L, Morocoima A, Aguilar CM, Gárate T, et al. Genetic variability of Trypanosoma cruzi TcI isolates from rural and urban areas of Venezuela. J Vector Borne Dis 2015; 52(1): 23–29.
44Herrera L, Urdaneta-Morales S. Didelphis marsupialis: a primary reservoir of Trypanosoma cruzi in urban areas of Caracas, Venezuela. Ann Trop Med Parasitol 1992; 68: 607–12.
45Ramsey JM, Gutiérrez-Cabrera AE, Salgado-Ramírez L, Peterson AT, Sánchez-Cordero, Ibarra-Cerden CN. Ecological Connectivity of Trypanosoma cruzi reservoirs and Triatoma pallidipennis Hosts in annthropogenic landscape with endemic Chagas Disease. PLOS One 2012; 7(9): e46013
46Levy MZ, Tustin A, Castillo-Neyra R, Mabud TS, Levy K, Barbu CM, et al. Bottlenecks in domestic animal populations can facilitate the emergence of Trypanosoma cruzi, the aetiological agent of Chagas disease. Proc Biol Sci 2015; 282(1810): 2014–2807.
47Conde Sangenis LH, Prates Nielebock MA, Carriello da Silva MC, Ribeiro Bento GM. Chagas disease transmission by consumption of game meat: systematic review. Rev Bras Epidemiol 2016; 19(4): 803–811.
48Castillo-Neyra R, Chou-Chu L, Quispe-Machaca V, Ancca-Juarez J, Malaga-Chavez FS, Bastos M. The potential of canine sentinels for reemerging Trypanosoma cruzi transmission. Prev Vet Med 2015; 120(3-4): 349–356.
49Gürtler RE, Cardinal MV. Reservoir host competence and the role of domestic and commensal hosts in the transmission of Trypanosoma cruzi. Acta Trop 2015; 151: 32–50.
50Jansen AM, Xavier S, Roque AL. The multiple and complex and changeable scenarios of the Trypanosoma cruzi transmission cycle in the sylvatic environment. Acta Trop 2015; 151: 1–15.
51Horwitz P, Wilcox, BA. Parasites, ecosystems and sustainability: an ecological and complex systems perspective. Int J Parasitol 2005; 35(7): 725–32.