Updated information of the dispersion dynamics of Chagas disease (CD) and a systemic analysis of these data will aid the early identification of areas that are vulnerable to transmission and enable efficient intervention. This work synthesized spatiotemporal information regarding triatomine fauna and analyzed this information in combination with the results from serological tests to elucidate the epidemiological panorama of CD in the state of Sergipe, Brazil. This is a retrospective analytical study that utilized information from the database of the National Chagas Disease Control Program. Between 2010 and 2016, 838 triatomines of eight species, namely,
Chagas disease (CD), which is a neglected disease caused by the protozoan
The Brazilian Ministry of Health published the II Brazilian Consensus on Chagas Disease with the objective of systematizing strategies for the diagnosis, treatment, prevention, and control of Chagas disease in the country and to reflect on the available scientific evidence [
The modes of transmission of the disease with epidemiological relevance are the consumption of contaminated food, blood transfusion, congenital acquisition, organ transplantation, and laboratory and vector accidents [
Despite the advances in vector control and quality assurance of blood transfusions in several Latin American countries, particularly through intergovernmental initiatives [
The early identification of areas with greater (or significant) vulnerability to the occurrence of synanthropic triatomines and transmission of human Chagas disease is fundamental for the design and application of efficient and economically viable intervention actions [
This retrospective analytical study utilized information registered in the database of the National Chagas Disease Control Program (
The northeast region of Brazil, which is one of the five geographical regions of the country, has an approximate population of 54 million inhabitants in an area of 1.3 million km2 and comprises nine states of the federation. This region is characterized by a small population density (41.48 inhabitants/km2), particularly in its rural areas. The northeast region is also one of the poorest regions of the country and remains very rural. In addition, this region presents the highest numbers of poor quality human dwellings, which are favorable for triatomine shelters.
The state of Sergipe, which is one of the 27 federative units of Brazil, is situated in the northeast region of the country. It is the smallest of the Brazilian states and occupies a territorial area of 21,915 km2 with an estimated population of approximately 2.3 million inhabitants (population density = 94.36 inhabitants/km2) [
Location of the municipalities and climatic divisions in the state of Sergipe, Brazil. Source: SEMARH-Sergipe [
The historical series of the presence of triatomines in the municipalities of the state of Sergipe from 2010 to 2016 were analyzed according to the species, the positivity to trypanosomatids, and the geographical distribution. The triatomines from each municipality were collected by endemic agents through manual inspection and capture at residential sites. The inspections were conducted based on reports from residents or a previously scheduled active search.
The insects were collected using the selective method, that is, manual search with metallic tweezers and a flashlight to inspect openings and dark places, with a collection time of one hour/housing unit/individual. Pirisa® chemical dislodger was used to force insects to leave their resting places. Some specimens were received by spontaneous demand. The triatomines were stored in screw-cap flasks and sent to the Laboratory of Entomology of LACEN accompanied by their identification form. In the laboratory, the triatomines were identified at the species level using key of Galvão [
The presence of flagellated trypanosomatids forms in fecal material was observed by removing the intestinal contents with scissors and forceps, macerated, and observed between slide and cover slip with one drop of buffered saline solution, using an optical microscope (400x magnification, running the entire cover slip). Two slides were prepared per examined specimen [
The distribution of triatomine occurrences by the municipality of the state of Sergipe was determined by the relative abundance of the triatomines found in each municipality and provides a dispersion trend for the triatomines in the territorial space of the state. The relative abundance (ra) is the percentage relation of the number of triatomines collected in the state (tt) with respect to the triatomines collected in the municipalities (tm) in the same period [ra(%) = (tm/tt) × 100] [
The Natural Infection Index was calculated to determine the potential risk of the municipality in relation to the transmission of Chagas disease. This index was calculated using the following equation:
We also analyzed the records of the Laboratory Environment Manager system (
Occurrence maps of triatomines and density (Kernel) were made representing the infestation and infection in the state (in the years 2010, 2012, and 2016), in addition to the percentages of positive serology for Chagas disease in the years 2012 and 2016, obtaining in this way the distribution in time and space. For the preparation of the maps, the free geoprocessing software Quantum GIS 2.18.15 (Free Software Foundation Inc.) was used.
The odds ratio was calculated for the presence of triatomines between the municipalities prioritized by the Housing Improvement Program and not prioritized. The Pearson correlation coefficient was also calculated relating the occurrence of triatomines and the Human Development Index (HDI) of municipalities. The tests were applied with the aid of the statistical software BioEstat 5.1 and adopting
The study was conducted in accordance with the ethical norms detailed in Resolution 466 of 12/12/2012 of the National Health Council and approved by the Ethics Committee of the Tiradentes University (Protocol no. 070309).
From 2010 to 2016, 838 triatomines of eight species, namely,
Distribution and climatic division of triatomines in the state of Sergipe, Brazil, from 2010 to 2016.
Triatomines collected between the years 2014 and 2016
Species |
Negative | Positive | ||||||||
---|---|---|---|---|---|---|---|---|---|---|
Nymphs | Female | Male | NI | Female | Male | Total | ||||
II | III | IV | V | |||||||
|
— | — | — | — | — | 1 | — | — | — | 1 |
|
— | — | — | — | 7 | 67 | — | 2 | 12 | 88 |
|
— | — | — | — | — | 1 | — | — | — | 1 |
|
1 | 4 | 4 | 5 | 11 | 14 | — | — | — | 37 |
|
— | — | 1 | — | — | 2 | — | — | 1 | |
|
— | — | — | — | 24 | 51 | 2 | — | 4 | 81 |
|
— | — | — | — | 5 | 4 | — | 1 | — | 10 |
Others |
51 |
All the collected species, which are considered vectors of CD, were previously described as occurring in the state of Sergipe by Dias et al. [
Additionally, Fonseca et al. [
From an epidemiological standpoint, the species
The distribution of triatomines in the state of Sergipe appears to follow a climatic pattern with a higher concentration in semiarid and agreste areas. The latter, which are characterized as transition zone, are bounded to the east by the Atlantic forest and to the west by the caatinga. However, the lack of a rigid delimitation between climatic areas and because of the anthropic influence in the coastal region of the state has led to some observations of triatomines in municipalities within a humid climate area.
The distribution of the number of triatomine notifications throughout the state decreased during the analyzed period; however, a progressive tendency in the concentration of notifications in the northern region of the state, which is the area of the São Francisco River Basin, could be observed (Figure
Spatial distribution (by density) of the percentage of infestation notification by triatomines in 2010, 2012, and 2016 in the state of Sergipe, Brazil. The hatching municipalities were considered at high risk for transmission of CD by the Sergipe State Health Department [
Between 2010 and 2016, thirty-two of the 75 municipalities in the state of Sergipe, that is, less than half, sent triatomine specimens for identification and analysis. In 2014, 60% of the triatomines captured in the state originated from the municipality of Tobias Barreto, followed by Canindé de São Francisco (8.7%), Porto da Folha (7.8%), and Gararu (6.8%).
According to the Chagas Disease Control Program of Sergipe, the following seven municipalities were classified as high risk for the transmission of the disease: Canindé de São Francisco, Poço Redondo, Aquidabã, Itabaiana, Itabaianinha, Ribeirópolis, and Lagarto [
Relative abundance of triatomines from 2010 to 2016 in the state of Sergipe, Brazil.
Risk |
Municipality | 2010 | 2011 | 2012 | 2013 | 2014 | 2015 | 2016 | Average period |
---|---|---|---|---|---|---|---|---|---|
High | Aquidabã | 1.04 | 0.00 | 1.35 | 1.94 | 4.85 | 1.28 | 2.78 | 1.89 |
Canindé São Francisco | 36.46 | 10.71 | 22.30 | 33.98 | 8.74 | 19.23 | 8.33 | 19.96 | |
Itabaianinha | 0.52 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.07 | |
Lagarto | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 2.78 | 0.40 | |
Poço Redondo | 19.79 | 34.29 | 20.95 | 9.71 | 0.00 | 0.00 | 2.78 | 12.50 | |
Ribeirópolis | 2.08 | 0.00 | 2.70 | 24.27 | 2.91 | 2.56 | 0.00 | 4.93 | |
|
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Medium | Cedro de São João | 0.52 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.07 |
Cumbe | 2.60 | 0.00 | 0.00 | 0.00 | 1.94 | 1.28 | 0.00 | 0.83 | |
Estancia | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 1.28 | 0.00 | 0.18 | |
Feira Nova | 1.04 | 0.00 | 0.00 | 0.00 | 1.94 | 0.00 | 0.00 | 0.43 | |
Frei Paulo | 0.52 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.07 | |
Gararu | 1.56 | 0.00 | 0.68 | 2.91 | 6.80 | 14.10 | 2.78 | 4.12 | |
Gracho Cardoso | 0.00 | 0.00 | 0.68 | 0.00 | 0.00 | 0.00 | 0.00 | 0.10 | |
Itabi | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 11.11 | 1.59 | |
Macambira | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 1.28 | 0.00 | 0.18 | |
Monte Alegre de Sergipe | 0.52 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.07 | |
Nossa Senhora Aparecida | 0.00 | 0.00 | 1.35 | 0.00 | 0.00 | 0.00 | 0.00 | 0.19 | |
Nossa Senhora da Gloria | 1.56 | 0.00 | 0.00 | 6.80 | 0.00 | 0.00 | 0.00 | 1.19 | |
Nossa Senhora de Lourdes | 0.52 | 0.00 | 0.00 | 0.00 | 0.97 | 1.28 | 0.00 | 0.40 | |
Pedra Mole | 0.00 | 0.00 | 0.68 | 0.00 | 0.00 | 0.00 | 0.00 | 0.10 | |
Pedrinhas | 0.00 | 0.71 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.10 | |
Poço Verde | 1.56 | 0.00 | 0.00 | 1.94 | 0.00 | 2.56 | 0.00 | 0.87 | |
Porto da Folha | 0.52 | 0.00 | 6.08 | 3.88 | 7.77 | 15.38 | 22.22 | 7.98 | |
Riachão do Dantas | 0.00 | 0.00 | 0.68 | 0.00 | 0.00 | 0.00 | 0.00 | 0.10 | |
Salgado | 0.52 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.07 | |
Santa Luzia do Itanhy | 0.00 | 0.00 | 0.68 | 0.00 | 0.00 | 0.00 | 0.00 | 0.10 | |
Simão Dias | 4.17 | 22.14 | 2.70 | 0.00 | 0.97 | 0.00 | 2.78 | 4.68 | |
Tobias Barreto | 18.23 | 26.43 | 38.51 | 14.56 | 60.19 | 38.46 | 38.89 | 33.61 | |
Tomar do Geru | 2.08 | 2.14 | 0.00 | 0.00 | 2.91 | 0.00 | 0.00 | 1.02 | |
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Low | Propriá | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 2.78 | 0.40 |
São Francisco | 1.56 | 2.14 | 0.68 | 0.00 | 0.00 | 0.00 | 2.78 | 1.02 | |
|
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UC | Pinhão | 1.56 | 1.43 | 0.00 | 0.00 | 0.00 | 1.28 | 0.00 | 0.61 |
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Total municipalities evaluated per year | 21 | 8 | 14 | 9 | 11 | 12 | 11 | — |
Of the evaluated municipalities, 48.5% performed systematic triatomine collections and evaluations at least twice (in at least two different years) in the analyzed period, whereas 27.3% performed these evaluations more regularly (four to seven times). It is noteworthy that the current disarticulation and instability in the surveillance and control of triatomines, particularly in northeast region of Brazil, are due to the decentralization of Brazilian endemic control programs and the discontinuation of National Health Foundation (
The epidemiological surveillance of the state of Sergipe has as a rule that encourages the population to notify the presence of suspected insects and to receive them through the Municipal Endemic Control. The routing of triatomines leads to a search (active search) in response to the notification and in the households where the triatomines were found; chemical control is carried out using insecticides of the pyrethroid class.
The Housing Improvement Program for the Control of Chagas Disease (
The municipalities that were prioritized for the program are Aquidabã, Itabaiana, Itabaianinha, Lagarto, Macambira, Poço Redondo, Ribeirópolis, and Umbaúba. These municipalities began to receive benefits before the period included in this study, and the actions of the program were concluded in 2016. The housing improvements aimed to reduce the possibility of triatomine colonization in the home and peridomicile environments and showed a potential reduction in the occurrence of vectors positive for
The municipalities that were not prioritized by the MHCDCh Program presented a 2.8-fold higher risk of triatomines observations than in the municipalities benefited by the Housing Improvement Program (OR = 2.842; CI = 0.873–9.644), which demonstrated that the building plastered brick houses and improvements outside the home reduce the possibility of triatomine detection.
The Human Development Index (HDI), which is calculated by the health, education, and income conditions of the population of the municipalities of the state of Sergipe, presented a negative and significant correlation with the presence of triatomines (
Among the municipalities with evaluated triatomines, 15 presented positivity for
Natural Infection Index (%) of triatomines by
Risk |
Municipality | 2010 | 2011 | 2012 | 2013 | 2014 | 2015 | 2016 | Average period |
---|---|---|---|---|---|---|---|---|---|
High | Aquidabã | 0.00 | — | 50.00 | 0.00 | 20.00 | 0.00 | 0.00 | 10.00 |
Canindé São Francisco | 8.57 | 20.00 | 6.06 | 2.86 | 0.00 | 0.00 | 33.33 | 10.12 | |
Poço Redondo | 10.53 | 6.25 | 6.45 | 10.00 | — | — | 0.00 | 4.75 | |
|
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Medium | Cedro de São João | 100.00 | — | — | — | — | — | — | 14.29 |
Cumbe | 60.00 | — | — | — | 0.00 | — | — | 8.57 | |
Gararu | 66.67 | — | 0.00 | 0.00 | 28.57 | 0.00 | 0.00 | 13.61 | |
Nossa Senhora da Gloria | 0.00 | — | — | 28.57 | — | — | — | 4.08 | |
Porto da Folha | 100.00 | — | 33.33 | 0.00 | 0.00 | 0.00 | 0.00 | 19.05 | |
Riachão do Dantas | — | — | 100.00 | — | — | — | — | 14.29 | |
Ribeirópolis | 25.00 | — | 25.00 | 0.00 | 0.00 | 0.00 | — | 7.14 | |
Salgado | 100.00 | — | — | — | — | — | — | 14.29 | |
Simão Dias | 0.00 | 9.68 | 0.00 | — | 0.00 | — | 100.00 | 15.67 | |
Tobias Barreto | 25.71 | 45.95 | 15.79 | 40.00 | 4.84 | 26.67 | 14.29 | 24.75 | |
|
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Low | São Francisco | 66.67 | 33.33 | 100.00 | — | — | — | 0.00 | 28.57 |
|
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UC | Pinhão | 33.33 | 100.00 | — | — | — | 0.00 | — | 19.05 |
Natural infections may be underreported due to the low sensitivity of routine methodology employed by the official control organs (optical microscopy) [
According to Dias and Coura [
This situation is also observed in other rural areas of the state and reflects an increase in the records of domiciled and peridomiciliary triatomines in historically nonendemic regions. This increase has altered the epidemiological dynamics of Chagas disease toward agreste and semiarid areas and increased the vulnerability of the population to chagasic infection (Figure
Geographic distribution (by density) of the percentage of cases of natural infection of triatomines by
Much of the interior of the state of Sergipe is characterized by small municipalities with a low population density (approximately 40 inhabitants/km2) and small rural properties intended for subsistence production [
The implementation of the GAL system by the Ministry of Health of Brazil permitted the centralization of information from the compulsory notification of diseases provided by the National System of Public Health Laboratories and supplied by epidemiological and analytical reports from regional networks of public health laboratories [
From the implementation of the GAL system in Sergipe to 2016, a total of 2,316 serological samples suspected of Chagas disease were analyzed in LACEN by indirect immunofluorescence for the detection of IgG antibodies to
Percentage of positive serology for Chagas disease in human patients based on the detection of IgG antibodies against
Risk |
Municipality | 2012 | 2013 | 2014 | 2015 | 2016 | Average period |
---|---|---|---|---|---|---|---|
High | Itabaiana | — | 0.00 | 0.00 | 20.00 | 0.00 | 4.00 |
Itabaianinha | 6.67 | 50.00 | 13.04 | 46.15 | 50.00 | 33.17 | |
Lagarto | 0.00 | 0.00 | 8.00 | 0.00 | 0.00 | 1.60 | |
|
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Medium | Arauá | 0.00 | 0.00 | — | 33.33 | — | 6.67 |
Boquim | 33.33 | 0.00 | 0.00 | 7.14 | 0.00 | 8.10 | |
Cristinápolis | 0.00 | 30.00 | 71.43 | 11.11 | 17.65 | 26.04 | |
Cumbe | 16.67 | — | — | — | — | 3.33 | |
Estancia | 11.54 | 8.79 | 10.96 | 1.96 | 9.09 | 8.47 | |
Indiaroba | 100.00 | 100.00 | 0.00 | 0.00 | 100.00 | 60.00 | |
Pedrinhas | — | 14.29 | 0.00 | 0.00 | 50.00 | 12.86 | |
Simão Dias | 33.33 | 50.00 | 33.33 | 20.00 | 33.33 | 34.00 | |
Tobias Barreto | 0.00 | 0.00 | 0.75 | 13.33 | 0.00 | 2.82 | |
Tomar do Geru | — | 33.33 | — | — | — | 6.67 | |
Umbauba | 100.00 | 5.26 | 19.23 | 9.57 | 37.14 | 34.24 | |
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Low | Itaporanga D’Ajuda | 0.00 | 16.67 | 33.33 | 0.00 | 25.00 | 15.00 |
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No risk | Brejo Grande | — | 100.00 | — | 0.00 | 0.00 | 20.00 |
Carmópolis | 0.00 | 100.00 | 0.00 | — | — | 20.00 | |
Japoatã | — | 50.00 | — | — | 0.00 | 10.00 | |
Nossa Senhora do Socorro | 0.00 | 0.00 | 15.38 | 11.11 | 20.00 | 9.30 | |
São Cristóvão | 0.00 | 0.00 | 0.00 | 16.67 | 0.00 | 3.33 | |
Aracaju | 4.76 | 8.47 | 6.25 | 14.81 | 5.71 | 8.00 | |
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UC | Pinhão | — | 25.00 | 0.00 | — | — | 5.00 |
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Total prevalence/year | 3.60 | 9.19 | 5.56 | 9.74 | 17.62 |
Population studies conducted in the south-central region of the state of Sergipe obtained varying prevalence rates for the adult population [
Serological investigations for CD in children under seven years are fundamental as indicators of new cases of vector transmission. In the state of Sergipe, Teles et al. [
In a serological survey conducted in the state of Piauí, in the northeast region of Brazil, Borges-Pereira et al. [
A relevant aspect with respect to the progression of CD is the existence of restrictive social policies and unequal production relations, which result in precarious housing in rural areas and easier access to food supplies and thus leading to the adaptation of triatomines to human dwellings. Thus, ecological, economic, and social determinants have made Chagas disease a public health problem, and for many years, this disease has been considered a “disease of poverty” [
Massaro et al. [
Sixty-four of the 75 municipalities in the state of Sergipe sent serum samples from suspected patients with CD in the evaluated period, and 22 were positive (Table
The municipalities located in the southern state of Sergipe revealed human cases with positive serology, which provide evidence of the presence of
Geographic distribution (by density) of the percentage of serological reagents for
Even though CD is considered a controlled disease, local revitalization of the Chagas Disease Control Program is necessary because this disease was observed in rural and periurban areas of Sergipe municipalities that were previously not considered at risk. Instead of neglect or discontinuity, this work supports timely action and optimization of human and structural resources for the surveillance and prevention of CD, particularly in the context of joint detection of human cases, intensification of anthropogenic actions, demographic growth, and the detection of various species of vectors and mammals with potential infection.
The need for both early diagnosis and adequate treatment of diagnosed patients (chronic cases) is predominant in a region in which the population is neglected due to their various difficulties in accessing basic healthcare, such as in the rural area of the southern center of Sergipe.
Our results show that the epidemiological panorama of Chagas disease in the state of Sergipe reveals a gradual increase of seroprevalence and is concentrated in the south-central part of the state with new notifications in the coastal region. The dispersion of domiciled triatomines (vectors) extends in the south-central direction to the north. Of the eight triatomines species registered in Sergipe during the period evaluated, seven were positive for
Thus, it is important to intensify the actions of Chagas Disease Control Program in Sergipe focused on the identification and intervention in new areas at risk of human transmission, considering the triatomine notifications in intra- or peridomicile and environmental conditions.
This first record of
The data that support the results of this study can be made available by official request to the corresponding author (C.M.M.). Some data are not publicly available because they contain information that may compromise the privacy of research participants. The following data related to the article can be accessed: 1. Situational report of Chagas disease in the state of Sergipe available at
The authors declare that there are no conflicts of interest regarding the publication of this article.
The authors thank the Laboratório Central de Saúde Pública do Estado de Sergipe (Central Laboratory of Public Health of Sergipe) (LACEN) for technical support. This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Apoio à Pesquisa e Inovação Tecnológica do Estado de Sergipe (Fapitec) (EDITAL CAPES/FAPITEC No. 10/2016—PROMOB Grant number 88881.157704/2017-01).