Date Published: January 19, 2017
Publisher: Public Library of Science
Author(s): Cynara Carvalho Parente, Fernando S. M. Bezerra, Plutarco I. Parente, Raimundo V. Dias-Neto, Samanta C. C. Xavier, Alberto N. Ramos, Filipe A. Carvalho-Costa, Marli M. Lima, Érika Martins Braga.
The aim of this work was to explore the potential risk of vector-borne Chagas disease in urban districts in northeastern Brazil, by analyzing the spatiotemporal distributions and natural infection rates with Trypanosoma cruzi of triatomine species captured in recent years. The main motivation of this work was an acute human case of Chagas disease reported in 2008 in the municipality of Sobral.
We analyzed data from community-based entomological surveillance carried out from 2010 to 2014. Triatomine natural T. cruzi infection was assessed by examination of insect feces by optical microscopy. Sites of triatomine capture were georeferenced through Google Earth and analyzed with ArcGIS. A total of 191 triatomines were collected, consisting of 82.2% Triatoma pseudomaculata, 7.9% Rhodnius nasutus, 5.8% T. brasiliensis, 3.7% Panstrongylus lutzi, and 0.5% P. megistus, with an overall natural infection index of 17.8%. Most infestations were reported in the districts of Dom José (36.2%), Padre Palhano (24.7%), and Alto do Cristo (10.6%). The overwhelming majority of insects (185/96.9%) were captured inside houses, and most insects tended to be collected in intermittent peaks. Moreover, captured triatomines tended to constitute colonies. The acute case reported in 2008 was found to be situated within a T. pseudomaculata hotspot.
The triatomine collection events carried out by dwellers were aggregated in time and space into distinct foci, suggesting that insects are intermittently and artificially introduced into the city, possibly via accidental migration from their natural reservoirs. The relatively high T. cruzi infection rate indicates considerable circulation of the parasite in these areas, increasing the risk of vector-borne Chagas disease infection. These data suggest a need to strengthen epidemiological surveillance and integrate appropriate control actions targeting triatomines, T. cruzi reservoirs, and human populations. Our data also identify Chagas disease transmission as a hazard in urban areas of Sobral.
Bloodsucking insects of the subfamily Triatominae are distributed widely throughout the Americas and are also vectors of the protozoan Trypanosoma cruzi, the causative agent of Chagas disease. Several triatomine species are of great epidemiological importance due to their high susceptibility to T. cruzi infection as well as their ability to invade and colonize households, the combination of which increases the risk of Chagas disease transmission. Chagas disease was first described by the Brazilian scientist and physician Carlos Chagas at the beginning of the 20th century . This disease has remained a serious public health problem in Latin America, where about 5 to 7 million people are currently infected, resulting in approximately 12,000 deaths annually . Chemical control of introduced/domiciled insect vectors, mainly Triatoma infestans , and progressive socioeconomic and housing improvement  have helped successfully interrupt vector-borne disease transmission in many regions. Thus, in the last few decades, most new cases in Brazil have corresponded to acute Chagas disease and have been associated with food-borne outbreaks. Such outbreaks have been a particular problem in northern Brazil (e.g. in the Amazon), where some juices have been contaminated with sylvatic triatomine feces containing T. cruzi [5,6,7]. In addition to acute infections, 1.9 to 4.6 million people are estimated to be chronically infected, approximately 1.0 to 2.4% of the Brazilian population, resulting in about 6,000 deaths annually . Chagas disease was endemic in the state of Ceará in northeastern Brazil , transmitted primarily by native triatomines migrating from the wild to dwellings. These triatomines are able to recolonize peridomiciles and intradomiciles shortly after insecticide control measures have been implemented [10,11], posing difficult challenges for Chagas disease control.
From 2010 to 2014, the residents of Sobral collected 191 triatomines, which were later laboratory-confirmed as the following species: Triatoma pseudomaculata (n = 157), Rhodnius nasutus (n = 15), T. brasiliensis (n = 11), Panstrongylus lutzi (n = 7), and Panstrongylus megistus (n = 1). The overall index of natural T. cruzi infection was 17.8%. The T. cruzi infection rates by insect species were as follows: T. pseudomaculata 17.8%, R. nasutus 13.3%, T. brasiliensis 9.1%, P. lutzi 28.6%, and P. megistus 0%. The insects were captured with similar frequencies in the dry (n = 97, 50.8%) and rainy (n = 94, 49.2%) seasons. Similarly, T. cruzi infection rates were similar in the dry (17 positive insects, 17.5%) and rainy (17 positive insects, 18.1%) seasons. Fig 3A and 3B shows the relationship between triatomine distribution and PIT locations where insects were collected in densely populated urban areas. R. nasutus was found mainly in the central and northern districts, while P. lutzi and T. brasiliensis were collected mainly in the central and northwestern areas. These geospatial analyses lead us to understand the extent to which vector distribution patterns are explained by actual infestation or community surveillance actions, so that meaningful lessons can be drawn from public health policies and interventions.
This study demonstrates the presence of urban spotlights of triatomines, vectors of Chagas disease, in densely populated neighborhoods of a city in northeastern Brazil. This finding represents a detailed account showing the presence of these insects in an urban environment, since Chagas disease is typically considered to be endemic in rural settings. Moreover, in northeastern Brazil, Chagas disease is usually thought to be transmitted by insects with natural reservoirs that invade and colonize houses from the wild . Therefore, Sobral seems to exhibit a unique eco-epidemiological scenario characterized by triatomine foci in informal urban settlements with substandard housing. These foci have the potential to produce acute Chagas disease cases, and represent a real risk to the population. This situation underscores interruption of vector-borne Chagas disease infection in this region as one of the main challenges of insecticide-based control policies. The triatomine collection events carried out by city dwellers were aggregated in both time and space, with insect collections restricted to only a few foci in the city. Moreover, T. pseudomaculata temporal peaks were detected, the largest of which was observed in 2010. This finding suggests that the insects are introduced into the city intermittently and artificially, and possibly undergo passive transport from their natural reservoirs (i.e., in the Caatinga biome that surrounds the city). Moreover, the acute Chagas disease case reported in 2008 was spatially related to these foci.
Sobral exhibits a unique eco-epidemiological situation, in which Chagas disease vectors are continuously present inside houses in different neighborhoods, thereby creating constant contact between humans and triatomines. This close contact presumably enables the emergence of Chagas disease cases. However, the frequency of this emergence is unknown, since acute T. cruzi infections are usually asymptomatic. A comprehensive investigation is urgently needed to determine which urban mammals are infected with T. cruzi and the seroprevalence of Chagas disease in the residents of this area. Community-based entomological surveillance must become a strategic component of Chagas disease control in this area, and will be strengthened by close involvement of major stakeholders, such as the residents themselves and the Sobral health authorities who should promote policies of assistance, surveillance and vector control. This cooperation between the population and local authorities will contribute decisively to avoid the emergence of new cases of the endemia.