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The main railroad and highway linking Rio de Janeiro with São Paulo pass nearby. Pop. () ,; () , This article was most recently revised.
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The entomological survey was carried out from July to November The various methods of capture included the use of battery-powered aspirators, mouth aspirators, Shannon traps, BG-Sentinel traps with and without dry ice and CDC light traps. Captured mosquitoes were separated, packaged and sent to the laboratory for sexing and molecular identification of the various species of anophelines.

The data were tabulated and analyzed using Microsoft Excel. Spatial analysis of the data was performed using ArcGis 10 software. In , 20 autochthonous cases and one imported case of malaria caused by Plasmodium vivax were diagnosed, with three cases of relapses. A total of mosquitoes were collected, of which were culicines and were anophelines. Nine species of genus Anopheles were identified, with the most abundant being An.

Spatial analysis of the data showed that the area could be considered to be at risk of malaria cases and that there was a high prevalence of Anopheles. The results presented indicate that this extra-Amazonian region has an environment conducive to maintenance of the malaria transmission cycle owing to the wide diversity of Anopheles species. This environment in combination with the high influx of people from endemic areas to the study area provides a perfect setting for the occurrence and maintenance of malaria.

Malaria is the most prevalent infectious disease caused by parasites in the world. On the South American continent, most cases occur in the Amazon region, and Brazil ranks fourth in terms of malaria prevalence, only behind Venezuela, Peru and Bolivia [ 2 ]. It is estimated that about 42 million people in Brazil are at risk of contracting malaria, and in more than , cases were registered [ 1 ], with Outbreaks of malaria have been reported in the regions for years.

Of this total, Among these, no autochthonous cases or deaths from the disease were registered [ 7 ]. Malaria is known to have a heteroxenous cycle, in which mosquitoes of the Anopheles genus are the biological vectors [ 1 , 3 ]. In Brazil, there are about 60 species of Anopheles [ 8 ], of which An. However, other species belonging to the subgenus Nyssorhynchus are also involved in the transmission of malaria in the Amazon, including An. In the extra-Amazonian region, An. Entomological identification of anophelines using traditional taxonomy is challenging since for many specimens it is impossible to determine the species using only the morphological characteristics of the mosquito; consequently, these species are grouped into complexes.

However, the development of molecular biology techniques has facilitated species identification through the use of various types of PCR analyses [ 11 ]. Beyond simple identification, new taxonomic regroupings have even been proposed using molecular biology, such as the one proposed by Foster et al. However, according to the latest Brazilan State records regarding species of Anopheles based on classical taxonomy, 11 species of the genus Anopheles have been recorded in the PB, four of which are potential malaria vectors: An. The municipality of Conde, similar to many others in the coastal regions of the Northeast, contains areas of mangrovew which are a transitional coastal ecosystem between the terrestrial and marine environments.

Species of Anopheles that reproduce in this environment exhibit a diverse pattern of behavior, feeding in peridomicile areas and resting in extradomicile ones [ 14 ]. In , this municipality recorded an epidemic of autochthonous malaria, leading the Ministry of Health to launch an epidemiological and entomological investigation into the factors involved in this epidemic. Understanding these factors are essential for explaining why malaria has returned to the Northeast and for ascertaining which risk factors may favor the maintenance of transmission in this municipality. An ecological study was carried out in the municipality of Conde, PB Brazil.

It is a locality covered by Atlantic Forest and is also well known for its beach tourism, welcoming many domestic and international tourists [ 15 ]. The colored circles in the inset at the top right identify the distribution of malaria cases by geolocation, with each green circle indicating one case; the yellow circle indicating one imported case from Venezuela, with relapse after treatment; the 3 orange circles indicating three cases that showed relapse after treatment; and the two red circles indicating residences where two cases were registered.

Epidemiological case data, such as sex, age, date of case report, date of first symptoms, clinical outcome, and place of occurrence, were gathered from case report forms made available by the Municipal Health Department. All cases were also georeferenced for the purpose of creating thematic maps and spatial analysis of data. Adult mosquitoes of genus Anopheles were collected at different locations points in Conde Fig. The various capture methods employed included a battery-powered aspirator Horst , mouth aspirator, the Shannon trap, BG-Sentinel traps, both with and without dry ice, and CDC-based light traps.

Five monthly collections were carried out during the study period, with each collection conducted for 3 consecutive days in intradomicile, peridomicile and extradomicile areas.

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The collection points were determined using the following criteria: places of residence of cases, places of residence close to those of cases and natural breeding sites for mosquitoes in the locality. The pentagons identify the distribution of 73 points where mosquito collections were performed, with white pentagons indicating investigated sites where Anopheles was not found and yellow pentagons indicating sampling sites or points of Anopheles collection.

The uppercase letters A—F refer to the six main neighborhoods where mosquitoes were collected and are described in caption to Fig. The collection of mosquitoes using the battery-powered aspirator was carried out in the intra- and peridomicile environments during the period when Anopheles hematophagy was at its greatest peak between 6 pm and 9 pm , with each aspiration lasting 20 min. Mosquitoes were collected with a mouth aspirator between 6 pm and 8 pm from the walls in peridomicile areas and the surface of Shannon traps installed in the extradomicile environment.

The variety of methods was used to increase the chances of catching mosquitoes, especially Anopheles , and to evaluate the best collection methods in this study area. After each collection, the mosquitoes were immobilized with ether, and anophelines were separated from culicines based on external morphological characters [ 14 ]. Some mosquitoes were damaged during collections and sorting, especially those captured using BG-Sentinel and CDC-based light traps.

Consequently, all anophelines were stored for species identification using molecular techniques DNA Barcoding. These specimens were stored in individual tubes containing silica gel that were labeled with location, time and method of collection. After sexing, each mosquito was sectioned, separating the head and chest including the legs and wings from the abdomen with the aid of sterile forceps and a scalpel.

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DNA was extracted from the thoracic segment including the legs and wings of each mosquito individually, in accordance to the alcohol precipitation protocol [ 16 ]. All forward and reverse sequences from each individual were analyzed in the CodonCode Aligner Program v. All mosquito collection sites, as well as all residences with cases of malaria registered in the municipality, were geo-referenced using a Vista Cx Garmin GPS Global Positioning System receiver Garmin Ltd.

Case data number of cases per residence, cases of relapse and imported cases and mosquitoes presence of Anopheles , density and diversity per capture location were incorporated into these spreadsheets, and thematic maps were created using the ArcGis 10 spatial data analysis software. Kernel density estimation KDE was used to identify areas of greatest spatial risk for malaria transmission in Conde. KDE analyses were performed using the following parameters: the Jenks natural breaks classification method; adaptive bandwidth the most suitable for analysis of local studies [ 19 , 20 ]; and unit area in square meters m 2.

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Municipal boundaries were used to determine the area marked out for analysis. The environmental background of the study area was examined using a satellite image from June , with high 0. This image is licensed under the Creative Commons Attribution 4. The first case was reported on 3 March , with symptoms reported to have started 1 week earlier 23 February The last case was reported on 22 October Among these 21 cases, three relapses were reported, including the imported case.

In addition, two of the cases were registered at the same residence. The distribution of cases by gender was practically the same, with 11 cases in men and 10 cases in women.

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The treatment regimen recommended by the Ministry of Health was adopted. This involves primary treatment of confirmed cases of P. Area A see Fig. In the five cases recorded in area C, two were in the same household and there was one relapse case The largest number of cases were recorded in area D, which was also the area in which the imported case with relapse occurred case The smallest number of cases were in those areas furthest from the beach E and F Fig.

During the study period, mosquitoes were collected, of which were culicines and anophelines. Nine species of anophelines were identified, the most abundant of which was An. Collection was performed at 73 points, and Anopheles mosquitoes were found at 16 of these Figure 3 shows the spatial distribution of Anopheles collection points and the abundance of mosquitoes at each point. The greatest abundance of Anopheles specimens were collected at collection points P6 and P16, with these two points together accounting for Figure 4 shows the diversity of mosquitoes at each capture point.

It is noteworthy that the points with the greatest abundance are also those with the greatest diversity of species and that An. Map showing representation of Anopheles density at each of the 16 collection points P1 — P16 , yellow pentagons. Anopheles density is represented by six pentagons that vary in size, ranging from 1 to Anopheles collected at one point. Map showing the diversity of Anopheles at each of the 16 collection points P1 — P Different Anopheles species are identified by colored circles, with different colors indicating different collection points.

The areas with the greatest risk of occurrence of malaria based on analysis of the distribution of cases and mosquitoes collected are identified in Fig. The highest concentration of cases was detected in area C, followed by area A. Areas B and D presented with a moderate risk for the occurrence of cases Fig. Analysis of the distribution of total Anopheles by collection points Fig. It is worth noting the existence of a second high-risk area for An. Maps showing the risk areas for occurrence of malaria and Anopheles as identified by kernel density estimation KDE. Hotspots are identified ona color scale from green to red low to high risk, respectively.

The colored circles identify the distribution of malaria cases by geolocation, with each green circle indicating one case; the yellow circle indicating one imported case from Venezuela, with relapse after treatment; the 3 orange circles indicating three cases that showed relapse after treatment; and the two red circles indicating residences where two cases were registered b KDE of Anopheles collection points total Anopheles.

The occurrence of autochthonous cases of malaria in Conde is concerning for epidemiological surveillance services, since the location—a beach tourist region that receives visitors from national and international areas endemic for malaria—has all the features required for transmission and local maintenance of the disease [ 21 ].

Furthermore, the Brazilian Northeast has already experienced a major malaria epidemic, when An. The mosquito was later eradicated by action undertaken by the Northeast Malaria Service, created in in cooperation with the Rockefeller Foundation [ 23 ].

This past history provides clear evidence that the Northeast of Brazil has an environment conducive to the introduction of exotic mosquito species, as well as to the maintenance of the diverse range of Anopheles species already present in the region. It is worth noting that Conde has a refugee program and voluntarily receives immigrants from Venezuela, a country with a high endemicity of malaria [ 1 ].

This may pose the risk of future introduction of new species of Plasmodium.

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Furthermore, the single imported case registered in the municipality during this outbreak of autochthonous cases did involve a Venezuelan immigrant recently arrived in the city. Upon arrival, this individual already exhibited symptoms of the disease and, as the epidemiological surveillance service was already effectively installed, diagnosis and treatment of the patient were immediate. However, this patient relapsed 2. Such relapses are common when the cause of the infection is P. There is therefore a risk of malaria epidemics occurring outside the Amazon region due to a large portion of the population no longer being immune to the pathogen [ 22 ].

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With the exception of the last case of relapse, the other cases occurred within the expected period for relapse, generally within 3—9 weeks after treatment, which is common for most strains of P. The last relapse occurred 5 months after the first diagnosis and, in this case, it may be that a new infection should be considered. However, it may also have been a relapse of the disease since P.

Local spread is suspected to have occurred after the Carnival festivities, which took place during the first week of March. The hypothesis is that some infected tourists initiated the cycle of the parasite when Anopheles mosquitoes became infected through hematophagy. As the P. The travelling habits of Brazilian population during periods of festivities and holidays may contribute to the occurrence of cases of malaria [ 26 ].

Most of the cases affected patients in early to mid-adulthood, even though malaria affects all age groups [ 27 ].