INTRODUCTION

Chagas disease, also known as American trypanosomiasis, has the flagellate protozoan Trypanosoma cruzi as its etiological agent¹, which is transmitted primarily by vector insects, the triatomines, which are hematophagous insects, belonging to the order Hemiptera, suborder Heteroptera, family Reduviidae, subfamily Triatominae^2,3,4.

According to the World Health Organization (WHO)⁵, about 6 to 7 million people are infected with T. cruzi worldwide, with Chagas disease found in endemic areas of 21 Latin American countries; however, it does not occur on the islands of the Caribbean. In Brazil, 4,287 deaths from this disease were recorded in 2019, with 1,937 only in the Southeast Region⁶. According to the Brazilian Ministry of Health⁷, from 2012 to 2016, 1,190 acute cases of Chagas disease were confirmed, and the North Region presented the highest number of cases, 97.1%.

In the world, 155 species of triatomines have been described, grouped into 18 genera and five tribes, with 68 species known in Brazil^7,8,9.

The Brazilian Northeast Region is considered of epidemiological importance¹⁰, as it presents large foci of transmission¹¹ and is divided into distinct physiographic regions that involve a diversity of 29 triatomine species^8,10. Triatoma brasiliensis and Triatoma pseudomaculata are considered native species of the region¹². In several municipalities in this region, the population has a high prevalence of infection by T. cruzi¹¹.

In Pernambuco State, 14 species of triatomines have already been found: Panstrongylus lutzi Neiva & Pinto, 1923; Panstrongylus megistus Burmeister, 1835; Rhodnius nasutus Stål, 1859; Rhodnius neglectus Lent, 1954; T. brasiliensis Neiva, 1911; Triatoma melanocephala Neiva & Pinto, 1923; Triatoma petrochiae Pinto & Barreto, 1925; T. pseudomaculata Correa & Espínola, 1964; Triatoma rubrofasciata (De Geer, 1773); Triatoma sordida (Stål, 1859); Triatoma tibiamaculata (Pinto, 1926); Rhodnius tertius (Lent & Jurberg, 1966); Panstrongylus geniculatus (Latreille, 1811); and Triatoma infestans (Klug, 1834). This last species was eliminated from the State after intense control activities, culminating in the certification of the interruption of vector transmission in Brazil^12,13,14,15. The species T. brasiliensis and T. pseudomaculata currently stand out as the main vectors of Chagas disease in the State, along with P. lutzi, which is also naturally infected by T. cruzi¹².

Recently, in Ibimirim, Pernambuco State, one of the most significant outbreaks of acute Chagas disease in Brazil was recorded, preliminarily associated with the ingestion of contaminated food, which resulted in 30 individuals being treated¹⁶.

Studies on the geographic distribution of triatomines are essential for understanding epidemiological aspects related to the transmission of T. cruzi and should be used to guide surveillance and control actions regarding Chagas disease¹³.

Therefore, the present study aimed to record the distribution of species of triatomines found in the home environment, between 2012 and 2017, in the VIII Regional Health Management (Gerência Regional de Saúde - GERES) of Pernambuco, which is constituted by priority municipalities for the control of Chagas disease in Pernambuco, and to identify the natural infection rate by flagellates morphologically similar to T. cruzi of the respective insects.

MATERIALS AND METHODS

This is a descriptive, quantitative, and retrospective study, with entomological data on triatomines collected from 2012 to 2017 at VIII GERES in Pernambuco.

Pernambuco has a territorial area of 98,076.021 km², an estimated population of 9,473,266 people, a population density of 89.62 inhabitants/km², and a Human Development Index of 0.673¹⁷. In all 184 municipalities of Pernambuco and on the island of Fernando de Noronha, 12 GERES, administrative units of the State Health Department, were created, each one responsible for a part of the cities, acting in a more localized way in primary care, in the restructuring of the hospital network, in municipal actions, and in the fight against infant mortality and various endemic diseases.

The VIII GERES is composed of seven municipalities (Figure 1), all belonging to the Sertão do São Francisco: Afrânio (8°30'54"S, 41°00'18"W), with a population of 17,586 inhabitants¹⁸; Cabrobó (8°30'51"S, 39°18'36"W), with a population of 30,873 inhabitants¹⁹; Dormentes (8°26'50"S, 40°46'16"W), with a population of 16,917 inhabitants²⁰; Lagoa Grande (8°59'49"S, 40°16'19"W), with a population of 22,760 inhabitants²¹; Orocó (8°37'06"S, 39°36'02"W), with a population of 13,180 inhabitants²²; Santa Maria da Boa Vista (8°48'28"S, 39°49'32"W), with a population of 39,435 inhabitants²³; and Petrolina (9°23'55"S, 40°30'3"W), a population of 293,962 inhabitants²⁴, where is located the headquarters of VIII GERES^12,25,26. These municipalities present the caatinga as primitive vegetation²⁷, with a total area of 14,654.862 km² and a semi-arid climate^28,29.

1: Afrânio; 2: Petrolina; 3: Dormentes; 4: Lagoa Grande; 5: Santa Maria da Boa Vista; 6: Orocó; 7 Cabrobó.

Figure 1 - Location of the municipalities of VIII GERES, Pernambuco State, Brazil 

In the municipalities of VIII GERES, triatomine control is carried out by chemical control (use of insecticides), together with active and passive surveillance, both in urban and rural areas. In the active surveillance, municipal agents to combat endemic diseases (ACE) visit the residences and collect the insects without prior notification to the resident, while, in passive surveillance, the residents themselves notify the ACEs to carry out the collection. The dwellings are structured with masonry walls with plaster, masonry without plaster, mud with plaster, mud without plaster, or wood. The roofs are made of tile, straw, wood, or metallic material.

The information used in the present study are from the database of the Chagas Disease Control Program (SISPCDCh) of Pernambuco State and refers to the triatomines collected in the households of the municipalities, identified and examined in the laboratory of VIII GERES, in Petrolina, and registered in the DOS-SISPCDCh System.

Insects were collected by municipal ACEs in households in urban and rural areas, using entomological tweezers and flashlights to inspect crevices and places devoid of lighting.

The triatomines were sent to the Regional Entomology Laboratory of VIII GERES for taxonomic identification and parasitological examination of infection by flagellates morphologically similar to T. cruzi. Triatomines were identified to species level according to Lent and Wygodzinsky³⁰ and Galvão and Dale³¹. The parasitological examination was performed by abdominal compression of triatomines, and the identification of parasites morphologically similar to T. cruzi was performed on slides stained with Giemsa and examined under an optical microscope (400X). The insects that presented incomplete data on the origin and natural infection were considered as exclusion criteria.

The natural infection rate was calculated using entomological indicators recommended by the Pan American Health Organization³²:

The maps were made using Microsoft Excel 2010 and QGIS v3.10. The study was approved by the Research Ethics Committee of the University of Pernambuco - CEP-PROPEGI, under number 3,376,395, on June 6, 2019.

RESULTS

In the period from 2012 to 2017, 9,738 specimens of triatomines from six species were collected: T. brasiliensis (8,251), T. pseudomaculata (1,323), P. lutzi (100), T. sordida (56), P. megistus (seven) e R. neglectus (one). P. lutzi, T. brasiliensis, and T. pseudomaculata were found in all municipalities in the Sertão de São Francisco. The infection rate for flagellates morphologically similar to T. cruzi in the examined triatomines was 2%. Of the six species collected, four were positive: P. lutzi, T. brasiliensis, T. pseudomaculata, and T. sordida (Table 1).

In Afrânio, specimens of five species of triatomines were collected, and it was the only municipality with a record of the R. neglectus species. Attention is drawn to the high rate of infection of P. lutzi (59.3%) by flagellates morphologically similar to T. cruzi in that municipality. Dormentes presented four species of triatomines, and P. lutzi had the highest infection rate (44.4%). In Lagoa Grande, the same species collected in Dormentes were found; however, the total infection rates differed: 1.0% and 3.3%, respectively. In Petrolina, five species of triatomines were collected, highlighting, once again, the high infection rate of P. lutzi (46.7%). Regarding the municipality of Santa Maria da Boa Vista, five species were identified, the same amount found in Petrolina, the greatest diversity of species. P. lutzi was also the species with the highest infection rate (20.6%) in Santa Maria da Boa Vista. Cabrobó and Orocó had three species each (Table 1).

T. brasiliensis was the only species that showed infection by flagellates morphologically similar to T. cruzi in all municipalities studied, while T. pseudomaculata was not infected only in Cabrobó. Overall, the highest infection rate was recorded for P. lutzi (38.0%) (Table 1).

The municipality of Petrolina had the highest amount of triatomines collected (3,420) and naturally infected insects (83). However, Dormentes had the highest infection rate (3.3%). Orocó had the lowest number of triatomines collected (182), while Cabrobó had the lowest infection rate by flagellates morphologically similar to T. cruzi (0.2%). The number of insects naturally infected by flagellates morphologically similar to T. cruzi by the municipality is shown in Table 1 and Figure 2.

In blue, the municipalities in Pernambuco that are not part of the VIII GERES.

Figure 2 - Distribution map of triatomines infected by flagellates morphologically similar to T. cruzi in the home environment in municipalities of VIII GERES, Pernambuco State, Brazil, between 2012 and 2017 

The year 2014 had the highest amount of triatomines collected (3,186). However, the year with the highest number of positive triatomines (67) and the highest infection rate for flagellates morphologically similar to T. cruzi (5.0%) was 2012 (Table 2).

In every year, T. brasiliensis was the most collected species: 2012 (357), in Afrânio; 2014 (707), in Lagoa Grande; and 2013 (605), 2015 (299), 2016 (496), and 2017 (496), in Petrolina. T. brasiliensis showed the highest positivity in Petrolina in the years 2012 (19), 2013 (13), 2014 (11), 2015 (18), and 2017 (10) (Table 2).

P. lutzi had the highest infection rates for five years: in 2012, 100.0% in Dormentes; in 2013 and 2014, in Afrânio, with 100.0% and 60.0%, respectively; and in 2015 and 2017, 100.0% in Petrolina. In 2013, T. pseudomaculata showed the highest infection rate for flagellates morphologically similar to T. cruzi in Orocó (100.0%). In 2016, the highest infection rate (12.5%) was detected in T. sordida in Petrolina, where the species was not found until 2012 (Table 2).

P. megistus was recorded in 2012 in Dormentes, Petrolina, and Santa Maria da Boa Vista and in 2014 in Afrânio, Lagoa Grande, and Santa Maria da Boa Vista. R. neglectus was recorded only in 2016, in Afrânio (Table 2).

DISCUSSION

CONCLUSION

Most of the species collected in VIII GERES of Pernambuco are common in the Caatinga biome. The present study contributes to health surveillance, as it found positive species in all municipalities in the Sertão de São Francisco, indicating the risk of vector transmission, with emphasis on P. lutzi, which had the highest infection rate for T. cruzi, and the municipalities of Dormentes and Petrolina that presented the highest positivity rates of the VIII GERES.