Occurrence of synanthropic triatomines ( Hemiptera : Reduviidae ) in the Federal District of Brazil

Introduction: Entomological surveillance of Chagas disease in the Federal District of Brazil (DF), has recorded the following triatomine species: Panstrongylus megistus, P. geniculatus, P. diasi, Rhodnius neglectus, Triatoma pseudomaculata, and T. sordida. We aimed to analyze the spatial and temporal occurrence of triatomine species collected in DF, and their indices of natural infection with trypanosomes. Methods: The Health State Secretariat of DF recorded triatomines between 2002 and 2010 in 20 administrative regions. This retrospective analysis considered the number of adults and nymphs of each species collected and infected in both intradomicile and peridomicile. Results: A total of 754 triatomines were collected in 252 reported domiciles. Panstrongylus megistus was the most frequent species (65%), followed by T. pseudomaculata (14%). Of the 309 examined insects, only 3 (1%) specimens of P. megistus were infected with flagellates morphologically similar to Trypanosoma cruzi. The spatial occurrence indicated a higher diversity of triatomines and frequency of T. sordida in rural areas. Moreover, there was a predominance of P. megistus in urban areas. The number of records of P. megistus in the rainy season was two times higher than that during the dry season. The largest number of triatomines was collected in November. Conclusions: The presence of P. megistus specimens infected with trypanosomes in domiciles, shows the potential risk of human infection in DF. Thus, it is essential to continue entomological surveillance, intensifying it in the rainy season and in regions of greater occurrence.


Article/Artigo
Entomological surveillance of Chagas disease in the Federal District of Brazil (DF), began in the 1980s with the establishment of triatomines information posts (PITs).These insects were sent to laboratory tests and were controlled with insecticides 1 .During this period the recorded species were Panstrongylus megistus (Burmeister, 1835), P. geniculatus (Latreille, 1811), P. diasi Pinto & Lent, 1946, Rhodnius neglectus Lent,  1954, Triatoma pseudomaculata Corrêa & Espínola, 1964, and T. sordida (Stål, 1859).In 1999, after the decentralization of health actions at The National Health Foundation (FUNASA), activities involving the research, control, and surveillance of triatomines began to be conducted by the Environmental Surveillance Directory (DIVAL) of the Health State Secretariat of Federal District (SES-DF).The surveillance maintains a community participation strategy with a network of 64 PITs in schools and health care units in the administrative regions of DF.
According to Knox and Oliveira 2 , P. megistus is the most widely distributed species in DF, followed by T. pseudomaculata, both recorded in intradomiciliary environments, thus drawing attention to a possible vectorial transmission of Trypanosoma cruzi to humans in DF, where autochthonous cases of Chagas disease have not been reported.
Studies on triatomines in wild environments have recorded R. neglectus and Psammolestes tertius Lent & Jurberg, 1965, in Mauritia flexuosa palm trees in DF 3,4 .Other studies have shown enzootic circulation of T. cruzi and T. rangeli in gallery forests.Indices of natural infection with T. cruzi were 33% for mammalian reservoir (Didelphis albiventris) and 9% for R. neglectus 5 , thus showing the need to maintain entomological surveillance and to monitor the invasion and/or colonization of wild triatomines in domestic environments.
Even without records of vectorial transmission of Chagas disease in DF, there is a possible relation between the human reservoir of T. cruzi (71,736 Chagas disease patients in DF, according to the latest serological survey) and synanthropic triatomines.Furthermore, the invasion and/or colonization of infected triatomines from wild ecotopes may represent the risk of vectorial transmission with the installation of peridomiciliary and domiciliary cycles of T. cruzi 6,7 .In this context, the objective of this paper is to analyze the spatial and temporal occurrence of triatomine species collected in DF, as well as their indices of natural infection with trypanosomes to direct actions of entomological surveillance of Chagas disease coordinated by SES-DF.

Study area
The Federal District of Brazil is geographically located between the parallels 15º30' and 16º03' south latitude, and between meridians 47°25' and 48°12' west longitude, in Central Brazil, one of the highest areas of the region, the Central Plateau.According to 2010 Census results, the population comprises 2,563,963 people in an area of 5,787,784km 2 divided into 30 administrative regions 8 .The area is filled with plateaus over 1,000m in altitude.The average annual rainfall is around 1,600mm, and the average annual temperature ranges between 18°C and 20°C with two distinct seasons, the dry season from May to September and the rainy season from October to April, the latter season with the highest temperature records 9 .

Triatomine collection and natural infection
The insects were collected in intradomiciliary and peridomiciliary environments by residents and then taken to the PITs.Each PIT receives a kit with materials for insect storage, a notepad to keep notes containing the address and location of collection, and tweezers for the handling of specimens.
After notification, the SES-DF public health agents did active searches in these houses and their annexes.The materials used for triatomine collection were metal tweezers and flashlights to inspect cracks and sites deprived of light; when necessary, dislodging liquid (Pirisa 2%) was applied.The insects were placed in polyethylene vials with shredded paper to better preserve them.The vials were properly numbered, tagged, and recorded on special forms of the Program for Chagas disease Control (PCDCh, SES-DF).
After collection, the insects were sent to the regional laboratory located at DIVAL for taxonomic identification 10 and for a search of natural infection by flagellates morphologically similar to T. cruzi.The parasitological search was carried out from abdominal compression and subsequent fecal examination of fresh sample, and from slides stained with Giemsa®, based on the manual of regulations on organization and operation of laboratories for diagnosis of Chagas disease 11 .The According to the reports provided by PCDCh, 754 triatomines were collected in 252 domiciles in DF between 2002 and 2010; on average, 84 triatomines were collected and 28 domiciles were reported per year.Eighty-one triatomines were not identified at species level due to poor preservation of specimens.Panstrongylus megistus was the most collected species (65%), followed by T. pseudomaculata (14%), T. sordida (8%), P. geniculatus (7%), R. neglectus (5%), and P. diasi (1%).In this same report, 117 triatomines did not present records from the environment of sampling and/or stages of development, and are not presented in Table 1.
Overall, 46% of triatomines were collected in intradomicile, these being adult insects more frequent in this environment (66%).In peridomicile there was a higher recorded frequency of nymphs (Table 1).In the group of 135 houses with a record of intradomiciliary infestation 16% presented triatomine colonization and 86 nymphs were collected, especially from P. megistus (66%).Colonies with up to 33 nymphs of P. megistus were also found in peridomicile.Among adults, the number of females was higher than that of males in both environments.
A relation was observed between the number of triatomines of each species that was collected and the location of occurrence (administrative regions of DF) (Friedman = 49.9;p<0.01); the largest number of collections was observed in Planaltina, a predominantly rural region, with the highest diversity of triatomines and frequency of T. sordida (Figure 1).In most of the other administrative regions visited domiciles were sprayed with insecticides by public health agents and were georeferenced by location with the support of geographical coordinates obtained with the Global Positioning System (GPS).
The analysis was based on occurrence data of triatomines between 2002 and 2010 in 20 administrative regions of DF, as supplied by PCDCh-SES-DF.For each recorded species, the total number of adults and nymphs collected and infected with flagellates morphologically similar to T. cruzi in intradomicile and peridomicile was analyzed.For statistical analysis, the number of triatomines collected from each identified species was related to the location of collection (administrative regions of DF) and to the month of collection by applying Friedman's nonparametric test (alpha = 0.01).
The tests were computed with Statistica®.there was predominance of P. megistus, this being the only species collected in urban areas like Park Way, Águas Claras, and Guará (Figure 1).By analyzing monthly data it was possible to observe that the number of triatomine records in the domiciliary environment during the rainy season (n=155) was higher than in the dry season (n=97).Considering only P. megistus (the most collected species in DF), the number of records during the rainy season (n=77) was two times higher than that during the dry season (n=38).The highest number of records occurred in November (Figure 2), which coincides with the onset of the rainy season.No significant differences were found between the number of triatomines collected from the other species over the months (Friedman = 11.8;p <0.37).

DISCUSSION
The results show that of the six species of triatomines collected in the domiciliary environment, P. megistus is the most important for epidemiological surveillance of Chagas disease in DF.In spite of the low indices for natural infection with trypanosomes for this species in DF, compared with studies in different regions of Brazil [12][13][14][15][16][17] , it is important to stress that some of the triatomines were found colonizing intradomicile and feeding on human blood according to precipitin tests (unpublished data), thus evidencing the risk of human infection.Our results also show that the spatial occurrence of triatomine species is different in the 20 administrative regions studied in DF, with the highest number of records and species richness observed in Planaltina, a predominantly rural region with the highest frequency of T. sordida.In most of the other administrative regions, areas with intense urbanization, a predominance of P. megistus was observed.The data also indicate that during the rainy season there are more records of triatomines, especially of P. megistus in November.
Between 1981 and 1996, a total of 4,007 specimens were recorded in DF, and the most collected species were P. megistus, T. pseudomaculata, R. neglectus, and T. sordida 1,2 .Our data show that P. megistus remains the most frequent species, followed by T. pseudomaculata, T. sordida, P. geniculatus, R. neglectus, and P. diasi.A study on the geographic distribution of synanthropic triatomines in the state of Goiás in the 1990s indicated the existence of five species: T. sordida, T. infestans, R. neglectus, P. megistus, and T. pseudomaculata 14 .The species with highest natural infection rate with trypanosomes was P. megistus, as observed in our study in DF.Between 2000 and 2003 four more species were reported in the State of Goiás: P. diasi, T. costalimai, P. geniculatus, and T. lenti 18 .As DF is geographically placed inside the State of Goiás, T. costalimai and T. lenti may also occur in wild environments in DF.Psammolestes tertius is found in some administrative regions of DF, in nests of Phacellodomus ruber birds, which are present in the crowns of M. flexuosa palm trees 4,19 .Even though natural and experimental infection of Ps. tertius with T. cruzi 20 had already been observed, the former species has strong association with wild birds 21 and, therefore, has low capacity of domiciliation.These behaviors may explain why Ps. tertius was never recorded by entomological surveillance in domiciles of DF 1,2 .It appears T. infestans never occurred in domiciles of DF as it has not been recorded since the beginning of entomological surveillance 1,2 .
Among the triatomine species found in Brazil, P. megistus presents different degrees of adaptation to the domestic environment.In the south of Brazil it occurs mainly in wild ecotopes 16,22 , unlike in the southeast and northeast regions where P. megistus has greater epidemiological importance for occupying artificial ecotopes 15,17,[23][24][25] .Specimens of P. megistus prefer tree hollows in arboreal habitats 26,27 , and they feed on marsupials (Didelphis spp.), which are frequently infected with T. cruzi, thus justifying high infection indices when compared with other species of triatomines 26,28,29 .A study on T. cruzi reservoirs in DF showed that specimens of D. albiventris are responsible for maintaining enzootic circulation of the parasite in the region, where 33% of these mammals were infected 5 .However, P. megistus has varied feeding habits, also feeding on birds, dogs, cats, rodents, cattle, goats, pigs, and humans 17,27,30 .Compared with other species such as T. sordida, P. megistus presents higher preferences for human blood, increasing the risk of transmission of T. cruzi by this vector 30 .
In the administrative regions of Park Way, Águas Claras, Sobradinho, Guará, and Taguatinga, areas with high urban densification 31 , P. megistus was the predominant species.Knox et al. 32 also reported the presence of P. megistus in DF in areas with intense anthropic pressure, but with remnants of native vegetation still left in ecological parks and gallery forests close to residences.The development of colonies of P. megistus occurs in humid environments 23,33 , and it is possible that gallery forests may be the natural habitat of populations of this species.With the disorganized growth of administrative regions many domiciles are found close to these areas, and this may favor dispersal by flight and domiciliary invasion of these triatomines, stimulated by environmental changes such as reduction of food sources in the wild environment, presence of food sources in peridomicile, and/or rising temperature 23,[33][34][35][36][37][38] .In this context, urban areas surrounded by remainder forests and with marked climate change over the year (as in DF) are likely to favor the invasion of P. megistus in artificial ecotopes.Future ecological studies of wild populations of P. megistus in gallery forests of DF may clarify these questions.At a later time, genetic analysis and morphological comparisons among wild, domestic, and peridomestic populations may contribute towards an understanding of the infestation dynamics of this species in the domiciliary environment of DF.
Our results indicate that the invasion of P. megistus specimens (mainly females) in domiciles of DF occurs more often during the rainy season, especially in November.The increased occurrence of adult specimens of P. megistus in the domiciliary environment over the last trimester of the year was observed in other studies in different regions of Brazil 30,37,39,40 , indicating that these triatomines present a higher potential to colonize domiciles and their annexes in the rainy season.In DF, this period is marked by an increase in temperature as from October 9 , which can stimulate the flight activity of P. megistus, as already observed for other species of triatomines 38,41 .The predominance of females in the domiciliary environment indicates their higher invasive potential in relation to males, which may be related to dispersion processes.A study on synanthropic triatomines in the state of Piauí showed that females of T. brasiliensis Neiva, 1911, and T. sordida were more frequently captured than males 42 , as observed for P. megistus and T. sordida in the present study.
Triatoma pseudomaculata was the second most collected species in DF.Unlike P. megistus, it lives under the barks of dead trees and in bird nests 27 , presenting lower indices of natural infection with T. cruzi 15 .This species was often found in domiciles in Planaltina and Paranoá, and in some of these domiciles nymphs were collected, indicating colonization.Even though T. pseudomaculata is more frequent in peridomicile and usually feeds on birds, the colonization in domiciles has been observed in Sobral, Ceará, and Berilo, Minas Gerais, suggesting adaptation of this species in this environment 25,43 .In the northeast of Brazil T. pseudomaculata has great importance for epidemiological surveillance of Chagas disease, its being the most frequent species after T. brasiliensis 15,42 .Some studies have suggested that the increasing presence of T. pseudomaculata in the domiciliary environment is related to climate change, deforestation, and cropland expansion 25,44 , which could explain the higher frequency of this species in the rural areas of Planaltina and Paranoá, observed in the present study.
Regardless of the fact that it has remained the most collected species in cerrado areas of Brazil for the past years 18,[45][46][47] , T. sordida presents a low risk of transmission of T. cruzi to humans because of its peridomiciliary behavior and marked ornithophily 15,34,[46][47] .Some studies show that zones of higher occurrence of T. sordida correspond to those of higher and older farm exploration 33 , which may justify the higher frequency of this species in Planaltina.
Rhodnius neglectus is widespread in central Brazil and has an important role in enzootic transmission of T. cruzi 5,7 .Apart from the invasion of adults in domiciles 48 , there is evidence of household infestation of R. neglectus (with bugs occasionally establishing breeding colonies) in the States of Minas Gerais, Goiás, and São Paulo 18,49,50 .R. neglectus occurs predominantly in wild environments, inhabiting different species of palm trees in Brazil [51][52][53] .In DF it can be found in M. flexuosa palm trees 3,4,19 , and sporadic occurrence in the administrative regions of Planaltina, Sobradinho, Ceilândia, and São Sebastião may be associated with the presence of palm trees in peridomicile.The role of these peridomiciliary palm trees in the maintenance of triatomines in DF should be evaluated in future studies.
Panstrongylus geniculatus occurred especially in Brazlândia, in the northwest region of DF, in agreement with the observations of Knox et al. 32 .In the wild environment P. geniculatus inhabits, preferentially, armadillo burrows (Dasypus spp.) 26,27 , but it has been found in the domiciliary environment in different states of Brazil 18,[54][55] .
Punctual distributions of P. diasi in DF were also observed.This species is distributed in areas of cerrado in central Brazil 18,56 and has been found in the domiciliary environment without description of wild ecotopes 26 .

FIGURE 1 -
FIGURE 1 -Number of triatomine bugs collected by species in 20 administrative regions of Federal District, Brazil, between 2002 and 2010.

FIGURE 2 -
FIGURE 2 -Number of specimens of Panstrongylus megistus collected throughout the year in domiciles of Federal District, Brazil, between January 2002 and December 2010.