Entomological survey in the state of Piauí, Northeastern Brazil, reveals intradomiciliary colonization of Triatoma brasiliensis macromelasoma.

This survey aimed to assess the presence of triatomine vectors of Chagas disease within the rural communities of São João do Piauí, Northeast Brazil. Intradomiciliary and peridomiciliary collection strategies were implemented wherein 279 specimens of Triatoma brasiliensis macromelasoma, both nymph and adult were found in 15 (50%) of the studied homes. Of the intradomiciliary insects, 73 (67.6%) were identified as nymph instars (1st instar [N1]= 6, N2= 14, N3= 28, N4= 7 and N5= 18). In the studied communities, a continuous interaction between triatomine bugs and humans could be shown. It is therefore urgent that suitable strategies for the control of the triatomine vector are implemented in this area.

INTRODUCTION

Chagas disease is caused by the protozoan Trypanosoma cruzi (Chagas, 1909), which persists zoonotically in the environment within several species of mammals and is transmitted by hematophagous insects called triatomines (Hemiptera, Reduviidae, Triatominae)[1,2]. In the past, control strategies for this disease have been implemented effectively in Brazil, such as the Control Program of Chagas Disease (PCDCh) which was established in 1975 by the extinct agency known as the Superintendency of Public Health Campaigns (SUCAM).

The actions of the program have successful and substantially reduced the incidence of the disease in main endemic areas. In 2006, Brazil was certified by the Pan American Health Organization/ World Health Organization as having succeeded in stopping the transmission of Chagas disease by its main vector, Triatoma infestans (Klug, 1834). T. infestans is an introduced vector and, as such, exhibits virtually no significant stocks in the sylvatic environment, making it vulnerable to targeted reduction, as achieved through PCDCh actions[3,4] with insecticides.

In Northeast Brazil, native triatomine species such as Triatoma brasiliensis (Neiva, 1911), among others, are the predominant vectors of Chagas disease[5-7]. Triatoma brasiliensis is a complex of seven species: i) T. brasiliensis, comprised of two subspecies [T. b. brasiliensis and T. b. macromelasoma (Galvão, 1956)], ii) T. juazeirensis (Costa & Felix, 2007, iii) T. sherlocki (Papa, Jurberg, Carcavallo, Cerqueira & Barata, 2002, iv) T. melanica (Neiva & Lent, 1941, v) T. lenti (Sherlock & Serafim, 1967, vi) T. bahiensis (Sherlock & Serafim, 1967, and vii) T. petrocchiae (Pinto & Barreto, 1925)[8,9].

These insects, which are capable of re-colonizing the domestic environment from wild stocks, represent an enormous challenge to the control of Chagas disease[10]. Consequently, reduction of entomological surveillance and domestic insecticide spraying practices can lead to the re-colonization of homes by triatomines. This, in turn, increases and protracts the human-triatomine contact, consequently producing new cases of Chagas disease[11].

The aims of this survey are to assess the presence of triatomine vectors both in and around domestic units of rural communities where vector control is intermittent in the State of Piauí, Northeast Brazil.

MATERIALS AND METHODS

The study was performed in 11 rural communities in São João do Piauí, Piauí State, Brazil (08°21’29” S/ 42°14’48” W’; altitude 222 m; human development index = 0.65) (see map in Figure 1), in December 2016 (beginning of rainy season). This municipality has 22,452 inhabitants dispersed over 1,532,432 km2 (population density = 14.65 inhabitants/ km2) in the Caatinga biome, with a semiarid climate, maximum temperatures range from 33 oC to 36 oC and minimum temperatures from 18 oC to 21 oC. The dry season runs from May to October (precipitation 31mm) and the rainy season runs from November to April (precipitation 625 mm). Active search and collection of triatomines by experienced agents was performed in areas both within and peripheral to the studied houses (intradomiciliary and peridomiciliary respectively). The study area included 30 houses in the communities of Grajal (n=3), Pedra D`Agua (n=2), Eugênio (n=8), Marrecas (n=1), Duque (n=1), Lagoa (n=1), Curral Velho (n=7), Santa Maria (n=1), Canto do Jepipapo (n=4), Espinheiro (n=1), and Lagoa da Serra (n=1). No dislodging substances were used.

Figure 1

Map of the state of Piauí, highlighting the municipality of São João do Piauí.

RESULTS

T. cruzi vectors were found in 15 (50%) domiciliary units. A total of 279 specimens were collected; 108 (38.8%) of these were intradomiciliary colonies (Figure 2A, arrow) characterized by the presence of all developmental instars of insects, including eggs (Figure 2B, arrow). Among intradomiciliary insects, 73 (67.6%) were nymphal instars: N1= 6, N2= 14, N3= 28, N4= 7 and N5= 18. Specimens were found in abundance beneath bed mattresses, and inside cracked mud walls (Figure 2A) as well as on the surface of plastered walls.

Figure 2

A, arrow. Triatomine nymphs and adults found colonising a house; B, arrow. Ocluded eggs of triatomines found in house interior; C. Highly engorged nymph found in the domestic environment.

Highly engorged insects were recovered from inside the houses (Figure 2C). Sixty-one adult insects (40 females and 21 males) were identified by taxonomic keys proposed by Costa et al. in 2014. Since all adults corresponded to T. b. macromelasoma (Figure 3), it was inferred that all immature specimens belonged to this species. Triatomines were also present in the peridomiciliary areas of houses, mainly in chicken huts and piles of tiles. The mean number of insects caught per household was 19.9 (range = 1 – 99; standard deviation (SD) = 26.2). The mean number of insects inside positive houses was 9.5 (range = 1 – 37; SD = 11.2). Among the studied houses, three were mud huts (pau-a-pique) and 27 were of brick construction. Table 1 summarizes the distribution of Chagas disease vectors by stage and community.

Figure 3

Triatoma brasiliensis macromelasoma adult collected in São João do Piauí.

Table 1

- Distribution of triatomines by community and instar in rural areas of São João do Piauí, State of Piauí, Brazil.

Community	Instar
	Female	Male	N1*	N2	N3	N4	N5	Total
Canto do Jenipapo	12	3	2	13	29	18	50	127
Curral Velho	4	3	0	1	6	1	5	20
Duque	6	4	3	6	13	2	11	45
Espinheiro	0	0	2	1	4	3	2	12
Eugenio	6	5	3	10	12	2	4	42
Lagoa	7	1	0	0	1	0	4	13
Lagoa da Serra	2	0	0	0	1	0	2	5
Pedra D'água	1	2	0	0	1	0	1	5
Santa Maria	2	3	0	0	0	0	5	10
Total	40**	21**	10	31	67	26	84	279

DISCUSSION

The present study demonstrates the presence of Chagas disease vectors in large densities within homes of several rural communities of São João do Piauí, Northeast Brazil.

The Southwest region of the State of Piauí where the studied communities are located has been recognized in the past as an endemic area to Chagas disease[12,13]. A seroepidemiological survey carried out in 2002 revealed that the prevalence rate of T. cruzi infection reached 11.6% in São João do Piauí, the highest in the State[12]. It is an area belonging to the caatinga biome, an environment favorable to the survival of members of the T. brasiliensis complex, as evidenced by its high relative densities in the region[14]. In Southwestern Piauí, the enzootic transmission cycle of T. cruzi has been demonstrated in wild mammals and domestic animals, such as dogs[15,16]. In the caatinga region, T. brasiliensis can be found in rock crevices, feeding on small mammals, their main source of food, and with which they share shelter from high local temperatures[7-17].

It is important to emphasize that Chagas disease control strategies, comprised of entomological surveillance and domestic insecticide spraying, have been discontinued in the study area. Indeed, the workforce of technicians and agents that implemented these practices has been diverted to projects of higher priority status, such as the control of the mosquito Aedes aegypti (Linnaeus, 1762).

The cessation of Chagas disease control activities in a region where the wild environment is favorable to the survival of important vectors such as T. brasiliensis, often leads to recolonization of peridomestic environments; mainly chicken coops and corrals[18]. In this case, vectors of Chagas disease are attracted from the forest by food sources represented by chickens, dogs and cats among others. This is exacerbated during the dry season when there are few wild animals available to serve as food sources in the forest.

Interestingly domestic colonization in the study area seems to occur independently of the existence of a link between the wild environment and the houses. Large intradomiciliary colonies were observed where human inhabitants were clearly serving as food sources for triatomines. Immature insect stages were frequently captured under bed mattresses and inside cracks in the walls of mud houses. This ecoepidemiological picture illustrates the risk of vector-borne transmission of Chagas disease in Southwestern Piauí.

According to occurrence data synthetized by Costa et al.[19], components of the T. brasiliensis complex have a relatively well defined geographic distribution; T. b. brasiliensis being more frequent in the States of Paraíba, Rio Grande do Norte, Ceará and Piauí; T. b. macromelasoma in Pernambuco; T. juazeirensis in Bahia; T. melanica in Minas Gerais; T. sherlocki seems to be restricted to Western Bahia. The studied area is situated in Southeastern Piauí, approximately 100 km from the border of Pernambuco State. Insects collected in this study were classified as T. b. macromelasoma. This is the second report of this subspecies in the State of Piauí[20].

In the State of Piauí, a comparison of the epidemiological situation before and after the control measures of PCDCh shows a positive impact, with a significant reduction in the seroprevalence rates between the 1970s and the early 21st century[14]. Nonetheless, two aspects should be emphasized: i) for 14 years no prevalence studies have been carried out so that the current knowledge regarding the transmission rate is lacking and ii) PCDCh has been discontinued in the majority of the State’s municipalities.

Data from this study reaffirm the need for the reimplementation of Chagas disease control activities in the State of Piauí as well as prevalence surveys in order to characterize the current Chagas disease morbidity pattern in the State.