Malaria epidemiology in the State of Piauí , Northeastern Brazil : a retrospective study with secondary data

Introduction: Malaria is not considered endemic in State of Piauí. Methods: Malaria epidemiology was examined using surveillance data. Results: During 2002-2013, of the 484 cases of malaria, 217 were classifi ed as probably acquired in Piauí, most frequently in the Campo Largo, Buriti dos Lopes, and Luzilândia municipalities, and 267 were considered probably imported, from the States of Pará, Maranhão, Amazonas, Roraima, and Rondônia. Probably-imported cases occurred throughout the year, while 80.2% of the probably-acquired cases occurred in April-August, peaking at the end of the rainy season. Conclusions: Malaria surveillance should be intensifi ed. Further ecoepidemiological and entomological studies are needed.

In 2014, 138,295 cases of malaria were recorded in Brazil, almost all of which occurred in the Amazon region.This region includes the States of Acre, Amapá, Amazonas, Maranhão, Mato Grosso, Pará, Rondônia, Roraima, and Tocantins (1) .Nevertheless, extra-Amazonian malaria cases have attracted the attention of the epidemiological surveillance system (2) .In Brazil, extra-Amazonian malaria cases can be attributed to the emigration of individuals with malaria from Amazonian states to nonendemic regions, introduction of Plasmodium into mosquito populations in receptive regions by parasitemic individuals coming from endemic regions, and/or transmission in the Atlantic Forest by the bromeliad mosquito Anopheles (Kerteszia) cruzii (2) .In Brazil, Plasmodium vivax and P. falciparum cause approximately 84% and 16% of all malaria cases, respectively (3) .
Patients with suspected malaria in endemic states are handled by an extensive network of governmental diagnostic and treatment centers (4) .Diagnosis is performed with Giemsastained thick blood smears, and antimalarial drugs are provided free of charge for any positive case.Usually, a second blood examination is provided after treatment to confi rm that the case was cured.The incidence of malaria has exhibited a downward trend in recent years, since more than 300,000 malaria cases were reported in 2009 (1) .However, major operational diffi culties persist, related with political issues, administrative gaps, and the unique ecological and socio-demographic characteristics of the Amazon region (5) (6) (7) .
The capacity to effectively manage malaria in the Brazilian Amazon is already present.Although few extra-Amazonian cases occur, they nevertheless represent an extremely important problem because they occur in regions in which the disease is poorly understood by both the population and health personnel (8) (9) (10) .This lack of understanding can delay diagnosis, increase the case fatality rate, and allow the persistence of parasitemic individuals in nonendemic areas.Some areas are potentially receptive to maintenance of autochthonous malaria transmission because they harbor Anopheles species that exhibit good vectorial capacity.In addition, many of these areas are vulnerable because of migrants with parasitemia from endemic regions.In this context, extra-Amazonian cases of malaria are becoming increasingly important and represent a major challenge to health authorities.
States in Northeastern Brazil, with the exception of Maranhão, which has part of its territory in the Amazon, are considered nonendemic and generally report only sporadic or imported malaria cases.As a result, limited data have been published regarding malaria in the State of Piauí.This study aimed to describe the epidemiological aspects of malaria in Piauí, with an emphasis on spatio-temporal trends.
The State of Piauí is located in the mid-northern region of northeastern Brazil.This region represents a confl uence of distinct biomes, specifi cally semiarid caatinga to the east, cerrado to the south, and pre-Amazonian rainforest to the west.Thus, the climate varies between tropical and semi-arid, with high temperatures ranging from 28 to 39°C.A marked rainy season occurs in the fi rst semester.Piauí has 3,194,718 inhabitants and an area greater than 251,577km 2 .The state has the lowest gross domestic product per capita in Brazil.Malaria is an obligatory notifi able disease in Brazil.Data from the System of Information for Notifi cation Diseases (SINAN) were retrospectively reviewed to characterize the geographic and temporal distributions of malaria cases reported in Piauí from 2002 to 2013.Each case was confi rmed by parasitological diagnosis using thick blood smears.Cases were included only if the Giemsa-stained thick blood smears were positive for P. vivax, P. falciparum, or P. malariae.Only malaria cases with well-established parasite-specifi c positive thick blood smears were included.
Climatic data were obtained from the National Meteorology Institute (INMET) at http://www.inmet.gov.br/(accessed April 15 th , 2015 at 2:00 PM).The maximum temperatures, minimum temperatures, and precipitation levels were retrieved; monthly averages were calculated for the 2002-2013 period.The selected climate data were obtained at an INMET station (3°27'40''S/42°22'18''W) near the cities at which the highest numbers of cases were recorded.
All suspected (probable) infection sites were reported on the notifi cation forms.However, it is not possible for the agents responsible for this information to perform a systematic search to defi nitively establish where each patient was infected with malaria.Agents are limited to asking where each patient has traveled in recent weeks and if he/she is returning from a known malaria-endemic region.Thus, in this study, cases were classifi ed into the following categories: probably acquired in Piauí, if the reported infection site was a municipality belonging to the State of Piauí, or probably imported, if the infection site reported in the notifi cation form was a municipality outside Piauí.
Malaria cases were distributed by month, year, geographic location (probable site of infection), and demographic characteristics.Spatial distribution was performed with QGIS (QGIS Development Team, available at http://www.qgis.org/en/site/).Statistical analyses were performed with SPSS® (IBM Corp., Armonk, NY, USA).Data are presented as descriptive statistics, and the characteristics of probably acquired versus probably imported cases were compared using the chi-square test.Statistical signifi cance was set at 5%.
This study was approved by the Ethics Research Committee at Oswaldo Cruz Institute/FIOCRUZ, license number 39405514700005248.
From 2002 to 2013, 484 parasitologically confi rmed cases of malaria were recorded.Of these, 217 cases were likely acquired in Piauí, and 267 cases were probably imported.The positive thick blood smear results were as follows: P. falciparum, n = 86 (17.8%);P. falciparum with gametocytes, n = 7 (1.4%);P. vivax, n = 362 (74.8%);P. falciparum + P. vivax, n = 25 (5.2%);P. vivax + P. falciparum gametocytes, n = 2 (0.4%); and P. falciparum gametocytes, n = 2 (0.4%).The proportions of infection with P. falciparum among the probably-acquired cases and probably-imported cases were 13.8% and 34.4%, respectively (p < 0.001).The monthly and annual distributions of malaria cases, including the variation in the proportions of P. falciparum infection, are shown in Figures 1A and 1B.While the probably-imported cases occurred throughout the year, 80.2% of the cases classifi ed as probably acquired occurred from April to August.A marked increase in the number of cases was observed in 2004.The climatic characteristics are displayed in Figure 2 and reveal that the number of the probably-acquired cases increased at the end of the rainy season in the state.
Extra-Amazonian cases of malaria have been reported in Brazil; consequently, the surveillance of such cases has increased (2) .Although the State of Piauí is situated outside the Amazon, it borders Maranhão and Tocantins, two states located in the Amazonian region.These two states have active transmission of malaria (11) (12) .
As presented here, Piauí records an average of approximately 40 malaria cases per year, nearly half of which are probably acquired in the state, i.e., are potentially autochthonous.Almost all of these cases were reported in the counties that border Maranhão; the Parnaíba River separates these two states.The middle-North region of Brazil is an extensive ecotone zone between the sub-humid pre-Amazonian region, Cerrado biome, and semi-arid Northeast.This region has an extensive network of drainage with the Parnaíba River as its main body of water.Piauí has remnants of the Atlantic Forest in its Northwestern region where many malaria cases were reported as well as in the central Southern region.
Entomological surveys performed in Piauí aimed at characterizing the local Anopheles species have provided interesting fi ndings.The most recent of these data were acquired from 2000 to 2010.These surveys reported the presence of the Anopheles species in the Amazon region (An.darlingi) and in northeastern Brazil (An.albitarsis, An. aquasalis), confi rming the transitional character of the middle-North region of Brazil.In this context, An. darlingi has been identifi ed in 85 municipalities ranging from the North to the South of Piauí, mainly in the western area of the state.An. albitarsis has been observed in 97 municipalities, mainly in Eastern Piauí, whereas An. aquasalis has been captured in two coastal municipalities in the north.Captures of primary malaria vectors have been documented in 50.2% of all the municipalities in Piauí (Coordenação de Vigilância em Saúde Ambiental/Secretaria de Estado de Saúde do Piauí, unpublished data).Similar data were reported in the State of Maranhão, illustrating the broad diversity of the Anopheles species in this transitional zone (13) .
The present study demonstrated that cases probably acquired in municipalities belonging to the state of Piauí exhibit distinct transmission dynamics of probably imported malaria.Moreover, a well-marked seasonality of probably autochthonous malaria was observed; specifi cally, the incidence increased at the end of the rainy season.Greater proportions of probably autochthonous cases compared with imported cases in women and children are also characteristic of this autochthonous pattern.Imported tend to occur more frequently in adult men, probably within an occupational context related to the migration of the workforce to and from Amazonian states in which malaria is endemic.The probable infection sites of most cases considered to be imported were in the South of Pará and in Rondônia, as well as in Manaus (the state capital of Amazonas) and Roraima.Thus, many subjects are likely to have been infected in areas with high incidences of malaria that are also associated with agriculture (including cattle raising), mining projects, and hydropower plant construction in the Amazon.These Amazonian areas continue to import members of the workforce from impoverished regions in northeastern Brazil.Many of these workers may have malaria when they return to their home cities in Piauí.Individuals with asymptomatic parasitemia coming from the Amazon can be an interface between introduced and autochthonous malaria because they represent a source of Plasmodium infection for the vectors.In this sense, the presence of parasitemic asymptomatic individuals during the period of increased vector density potentially produces autochthonous cases.The importance of asymptomatic and submicroscopic infections for transmission maintenance, as well as the need to improve diagnostic tools, has been demonstrated in different regions, as recently reviewed by Bousema et al. (14) .In this sense, Piauí is particularly receptive to malaria, as well as quite vulnerable due to its proximity to endemic states and the migratory fl ux of workers to the Amazon.

Nascimento
JAA et al. -Malaria in the State of Piauí

RevFIGURE 1 -
FIGURE 1 -Monthly distributions, annual distributions, and proportions of malaria cases caused by Plasmodium falciparum reported in the State of Piauí, Northeastern Brazil, between 2002 and 2013.