Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 556–562

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Tropical Medicine and Hygiene
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Increasing incidence of malaria in the Negro River basin,

Brazilian Amazon
A.C. Cabral a , N.F. Fé b , M.C. Suárez-Mutis a , M.N. Bóia a,c , F.A. Carvalho-Costa a,∗
a
Oswaldo Cruz Institute, Oswaldo Cruz Foundation, Ministry of Health, Rio de Janeiro, Brazil
b
Gerency of Entomology, Amazonas Foundation for Tropical Medicine, Amazonas, Brazil
c
Faculty of Medical Sciences, Rio de Janeiro State University, Rio de Janeiro, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Malaria in Brazil is virtually restricted to the Amazon Region, where it has a heterogeneous
Received 3 March 2009 geographic distribution. We reviewed secondary data in order to describe the regional
Received in revised form 26 March 2010
and temporal distribution of 8018 malaria cases seen between 2003 and 2007 in Santa
Accepted 26 March 2010
Isabel do Rio Negro, a municipality in the northwest Brazilian Amazon. A significant rise in
Available online 11 May 2010
malaria incidence, mainly in the Yanomami Indian reservation, was observed during this
time. Anopheline breeding sites were also mapped and entomological data were obtained
Keywords:
through the capture of larval and adult mosquitoes. Thirty-three potential breeding sites
Malaria
Amazon were identified in the urban and periurban areas, 28 of which were positive for anopheline
Anopheles darlingi larvae. Anopheles darlingi specimens were captured in both intra- and peridomicile locations
Yanomami Indians in the urban areas. Demographic data were also assessed via a sectional survey, revealing
Plasmodium vivax that the majority of dwellings were vulnerable to mosquitoes. This study suggests that
Plasmodium falciparum urban and periurban areas of this municipality are highly susceptible to epidemic malaria,
which is endemic in the Yanomami Indian reservation near the city. In addition, trans-
mission can be perpetuated autochthonously in the urban area, drawing attention to the
continuous need for preventative measures such as controlling adult and aquatic stages of
mosquitoes and improving housing.
© 2010 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All
rights reserved.

1. Introduction Within the Amazon, some areas are considered to have

Malaria in Brazil is virtually restricted to the Amazon
Region, where a heterogeneous geographic distribution
is observed.1–3 Since the 1960 s, when control programs
reduced the incidence to 50 000 cases per year and confined
its transmission to Amazonian Brazil, malaria has been
increasing progressively in this region.3 About 600 000
malaria cases occur annually in the Amazon Region; nearly
80% are caused by Plasmodium vivax, with the remainder
being caused by Plasmodium falciparum.4
∗ Corresponding author. Present address: Av. Brasil 4365, Pav. Leônidas
Deane, Sala 308; CEP 21045-900, Rio de Janeiro, Brazil.
E-mail address: guaratiba@ioc.fiocruz.br (F.A. Carvalho-Costa).
unstable or epidemic malaria, while other regions have
an endemic or stable pattern of transmission.3,5,6 The
main species of mosquito responsible for malaria trans-
mission in Brazil is Anopheles darlingi, which is highly
anthropophilic.7,8 At least 33 species of anophelines exist in
the Amazon region,7–9 and other species of minor epidemi-
ologic importance that have been found to be infected with
Plasmodium include An. triannulatus, An. mattogrossensis,
An. nuneztovari, An. braziliensis, An. peryassui, An. mediop-
unctatus, An. albitarsis, An. galvaoi, An. aquasalis, and An.
Strodei.9,10
Controlling malaria in the Brazilian Amazon has repre-
sented a real challenge to health authorities due to several
factors, including the difficulty of maintaining preventative
measures in many Amazonian communities, mining, the

0035-9203/$ – see front matter © 2010 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.trstmh.2010.03.008
 A.C. Cabral et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 556–562
construction of roads and dams, and colonization programs
and migrations.1–4 The latter two factors especially have
concentrated the population at the expense of adequate
sanitary infrastructure due to disordered and unplanned
urbanization, which has favored the development of artifi-
cial anopheline breeding sites.11 In addition, asymptomatic
individuals with low parasitemias living in endemic areas
often contribute to malaria transmission without being
aware that they are infected.5,12–14
The Negro River Basin is one of the most preserved and
least populated Amazonian regions, containing four munic-
ipalities. Although some of the Amerindian-descended
inhabitants still live in hundreds of small riverine com-
munities, an ongoing trend of migration towards the
incipient urban centers has become apparent. In the 1990 s,
many Indian reservations were demarcated in this area.
Among these reservations, the Yanomami Indian reserva-
tion encompasses 96 650 km2 of territory. It is part of three
municipalities in the state of Amazonas, all of which are
located in the Negro River Basin.
Recent studies near the Padauiri River, a tributary of the
Negro River, have revealed fluctuation of incidence rates
of malaria and periodic changes in its etiological profile.15
Other studies have also demonstrated the importance of
subclinical infections in the Negro River Basin.5,13 How-
ever, little information exists about malaria transmission in
this region. This study therefore aimed to obtain epidemi-
ological, entomological and demographic data related to
malaria in Santa Isabel do Rio Negro, a municipality located
in the upper Negro River region.
2. Methods
2.1. Setting and population
This study was performed in Santa Isabel do Rio Negro,
a municipality situated in the northwest region of the state
of Amazonas (0◦ 28 S and 65◦ 32 W). Santa Isabel do
Rio Negro is located 781 km from the capital of Amazonas,
Manaus, by fluvial route via the Negro River. The majority of
the population is of Amerindian ancestry, but diverse eth-
nic heritage is also present, mainly in the urban/periurban
areas. The whole municipality has 7712 inhabitants dis-
tributed over 63 127.2 km2 . The urban region has 4220
inhabitants, who reside in 773 dwellings distributed among
six districts. The remaining residents are distributed in
patches along small riverine communities in the backlands
of the municipality. This population includes 1393 people
who live on the Yanomami reservation. The Yanomami are
semi-nomadic Indians living in communities widely dis-
persed throughout Amazonian Venezuela and Brazil. Eight
Indian villages, called xaponos, are situated in Santa Isabel
do Rio Negro; Yanomami Indians are relatively isolated
from Brazilian society and preserve their culture and lan-
guage (see map in Figure 1). Riverine communities depend
on subsistence farming, fishing and forestry. Inhabitants
of the urban/periurban areas and non-Yanomami river-
ine communities descend from Tukano Oriental-speaking
(which includes Tukano, Pira-tapuya, and Desana ethnic
groups) and Arawak-speaking (Baniwa, Baré, and Tari-
ana ethnic groups) societies. In contrast to the Yanomami
557
people, this multiethnic society was assimilated and accul-
turated to the occidental life style and Christian religion, a
process stimulated by Catholic missionaries who arrived in
the region around one century ago.
2.2. Secondary data gathering
Malaria is an obligatory notifiable disease in Brazil.
Secondary data from the National Malaria Epidemio-
logic Surveillance System databank (SIVEP/Malaria) were
reviewed to characterize the geographic and temporal dis-
tribution of 8018 cases of malaria. Each of these cases was
registered between 2003 and 2007 and also confirmed
by parasitological diagnosis. There was no change in the
methods of estimating the number of malaria cases from
2003 to 2007. In order to perform malaria surveillance, the
Brazilian Ministry of Health maintains a network of labo-
ratories distributed throughout the Amazonian region, and
every municipality possesses at least one branch at which
cases can be notified. This system aims to assess every
malaria case through both passive and active surveillances.
Thick blood smears are performed by trained personnel,
and case definitions are the same for both active and
passive surveillances. Cases are included in the databank
only if the Giemsa-stained thick blood smears are pos-
itive for P. vivax, P. falciparum, or P. malariae. Although
standard Giemsa-stained thick blood smears are not sen-
sitive enough to detect cases of malaria when parasitemia
is low, they remain the standard detection technique in
many countries because of their practicality and low cost.
Anti malarial drugs – distributed exclusively by the malaria
surveillance system – are provided in blisters, free of charge
for any positive case, and a second blood smear is per-
formed after treatment to confirm that the patient is cured.
Brazilian health authorities can access the databank at
http://portalweb04.saude.gov.br/sivep malaria/. The data
base provides the following information for each locality
(e.g., village, district, road etc.): (i) number of cases, (ii)
place of infection of the cases, (iii) month, (iv) species of
Plasmodium, (v) place of residence of the infected indi-
vidual, (vi) rate of cases caused by P. falciparum, and (vii)
annual parasitary incidence/1000 inhabitants (API).
In order to characterize the geographic distribution of
malaria cases, the municipality was divided into four zones:
(i) urban/periurban (six districts, population 4220
inhabitants; further subdivided into three areas: farms con-
tiguous to the city, peripheral districts and central districts
[Figure 1]), (ii) Yanomami Indian reservation (eight vil-
lages, 1393 inhabitants), (iii) riverine communities around
the town (35 villages, 782 inhabitants) and (iv) riverine
communities far from the town (14 villages, 1317 inhab-
itants).
2.3. Demographic survey
The characteristics of the dwellings and demographic
data were assessed through a cross-sectional survey car-
ried out in September 2007. One hundred and thirty-six
families (17.5%) out of the 773 living in the urban/periurban
zone were surveyed. Sampling was performed randomly
and included residents from all districts in these areas. A
558 A.C. Cabral et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 556–562

Figure 1. Study area and anopheline breeding sites mapped in urban and periurban zones. Legend: A = Yanomami Indian Reservation, B = riverine commu-
nities near the city, C = riverine communities far from the city, D1 = urban area, central districts, D2 = urban area, peripheral districts, D3 = periurban area
(roads and farms). Black points = anopheline breeding sites.

questionnaire was used to assess knowledge about malaria
transmission and prevention, learn characteristics of the
dwellings relevant to their vulnerability to mosquitoes and
obtain data on travels or visits to hyperendemic zones.
Interviews were performed after written consent was given
by the head of the family. The sample size for the main
municipal area was stipulated by estimating a rate of
50% for the variable examined and an acceptable error
of 5%.
2.4. Entomological survey
Urban and periurban anopheline breeding sites were
identified by examining samples from water collection
sites for immature mosquito stages. Two surveys were car-
ried out: the first in July 2006 and the second in September
2007. All of the 33 breeding sites identified were examined,
with between 20 and 30 water samples obtained from each
site. A standardized 500 mL entomological dipper provided
by the Brazilian Health Surveillance Agency was used to
obtain representative samples of larval mosquitoes. Col-
lected larvae were transferred to 5 mL tubes with ethanol
70% and examined in a microscope within 12 hours of cap-
ture. The identification keys used were from Consoli and
Lourenço-de-Oliveira.16
Adult mosquitoes were captured using human bait and
a manual aspirator. The individuals who operated the
aspirators were trained members of the research team; fur-
thermore, mosquito captures were always performed by
these same members. Collections were carried out from
6:00 p.m. to 9:00 p.m. using human bait both inside and
around the outside of houses. Specimens were addition-
ally caught with two CDC type traps equipped with an
incandescent light bulb (Centers for Disease Control; CDC
miniature light trap model #2836, BioQuip Products, Inc.,
Rancho Dominguez, CA, U.S.A.: http://www.bioquip.com).
Each CDC trap was positioned indoors, one meter above
ground level, and left for a 12-hour period (6:00 p.m. to
6:00 a.m.).
3. Results
3.1. Regional and temporal distribution of malaria cases
The absolute number of malaria cases rose more than
sixteen times from 2003 to 2007 (Table 1). Additionally, a
shift in the geographic distribution of cases was observed:
the Yanomami reservation housed only 20% of the identi-
fied malaria cases in this region in 2003, but it contained
80.8% of them by 2006 and 66.7% by 2007 (Table 1). The
 A.C. Cabral et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 556–562 559

Table 1
Malaria cases, annual parasitary incidence (API)/1000 inhabitants, and P. falciparum/P. vivax (P.f./P.v.) ratio in Santa Isabel do Rio Negro, Amazonas, from
2003 to 2007 by zone

2003 2004 2005 2006 2007

Zone Cases API P.f./P.v. Cases API P.f./P.v. Cases API P.f./P.v. Cases API P.f./P.v. Cases API P.f./P.v.

Urban/periurban 81 19.2 0.20 62 14.7 0.06 26 6.2 0.18 73 17.3 0.14 537 127.2 0.20
Yanomami Indian 59 42.3 0 297 213.2 0.24 717 514.8 0.13 1326 951.9 0.16 3219 2310.8 0.85
Reservation
Riverine communities 37 47.3 0 15 19.1 0.36 36 46.0 0.12 86 109.9 0.03 293 374.6 0.031
near the town
Riverine communities 124 94.1 0.14 40 30.3 0.33 60 45.5 0.15 155 117.6 0.07 775 588.4 0.19
distant from the town

Figure 2. Malaria cases notified in Santa Isabel do Rio Negro from 2003 to 2007, by zone.

API in this area also rose from 42.3 in 2003 to 2310.8 in
2007. Furthermore, the P. falciparum/P. vivax (P.f./P.v.) ratio
increased substantially in this zone.
An increase in malaria incidence was also observed in
the urban and periurban areas of the municipality in 2007,
when 537 cases were identified (Table 1, Figure 2). In these
zones, the API increased from 19.2 in 2003 to 127.2 in 2007.
The major sites of infection in the periurban area were iden-
tified as the roads leading to farms. In 2007, these farms
were the first places where malaria cases were noticed,
after which additional cases were subsequently seen in the
peripheral and central districts (Figure 3).
3.2. Demographic survey
Gaps permitting the entry of mosquitoes were observed
in 53% of the dwellings in the urban/periurban zones. Addi-
tionally, spaces were present between the floor and the
walls and between the walls and the roof in 15% and 46% of
the houses, respectively. Among the families surveyed, 54%
regularly visited farms in the periurban area; furthermore,
39% of the heads of the families studied did not know how
malaria was transmitted (Table 2).
3.3. Entomological survey

Mapping studies showed that insect breeding sites

were located mainly in the peripheral urban districts and
near the periurban roads; furthermore, the locations of
the insect breeding sites corresponded to the locations of
the majority of the cases in the outbreak. Of the water
bodies analyzed, 85% (n = 28) were positive for Anophe-
les larvae. Furthermore, aquatic stages of An. darlingi, An.
triannulatus, An. albitarsis, An. mediopunctatus, An. nunez-
tovari and An. peryassui were also identified (Figure 1).
Fourteen adult An. darlingi specimens were collected in
urban (one in intradomicile, four in peridomicile) and
Figure 3. Geographic and monthly distribution of urban/periurban
periurban (four in intradomicile, five in peridomicile)
malaria cases in 2007. areas.
560 A.C. Cabral et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 556–562
Table 2
Socio-demographic characteristics relative to malaria transmission in 136
families in Santa Isabel do Rio Negro, 2007 [n (%) = absolute (proportional)
numbers].
Socio-demographic characteristics
House characteristics
Uncompleted house structure (lacking walls)
Presence of slits
No junction between floor and walls
No junction between walls and roof
Did not know how malaria is transmitted
Did not know how malaria is prevented
Frequent the Yanomami reservation
Frequent farms in the periurban area
Used to prevent malaria
Bed net
Fan
Insecticide
Window net
4. Discussion
This survey aimed to identify factors relating malaria
epidemiology to ecology in the Negro River basin, a
sub-region of the Brazilian Amazon. A major limitation
associated with using secondary data based on tradi-
tional parasitological diagnoses is their underestimation
of malaria cases and, consequently, of actual incidence
rates. Despite this limitation, however, this analysis of
malaria cases reported from 2003–2007 generated valu-
able insights into the distribution of the notified cases
within the municipality.
Malaria incidence rose in the state of Amazonas from
2002 to 2005 and subsequently decreased from 2005 to
2007; however, the sharp decline of malaria incidence
between 2005 and 2007 in the state of Amazonas did not
occur at the micro-regional level of the upper Negro River
basin. Rather, the main finding of our work is that both
the absolute number of cases and the API increased sig-
nificantly from 2003 to 2007 in the upper Negro River.
This finding is important because this diverse municipality
includes urban and periurban areas, riverine communities,
and also the Yanomami Indian reservation. Out of these
four defined sub-regions of the studied municipality, the
API increased 6.7 times in the urban/periurban areas and
a staggering 55 times in the Yanomami reservation from
2003 through 2007.
Although malaria occurs in all Brazilian Amazo-
nian states, a very heterogeneous distribution has been
observed: 90 municipalities, belonging to three states
(Acre, Amazonas and Rondônia) are considered high risk
areas (API greater than 50).17 Furthermore, the studied
municipality belongs to this high risk area. This focal
pattern of malaria epidemiology in the Amazon region sug-
gests that intrinsic local socio-environmental factors play
the greatest role in malaria transmission. Many of these
factors are well-identified, such as deforestation resulting
from development projects, mining activities, cattle ranch-
ing and the construction of power plants.1,2,18 However, the
increase in malaria incidence in Santa Isabel do Rio Negro
does not seem to be related to such factors, since no mining
projects have been undertaken in this region. In addition,
no new agricultural or other developmental projects have
recently begun in this region. We argue that a lack of atten-
tion to preventative measures, combined with an envi-
ronment conducive to malaria transmission, have allowed
n (%) malaria to re-emerge and reach hyperendemic levels.
Malaria was first introduced to the Yanomami popu-
7 (5.1) lation by clandestine gold miners by the 1980 s and now
72 (53)
represents a major public health threat for these indi-
20 (15)
63 (46) viduals; however, an extensive active surveillance and
53 (39) treatment system implemented in 2000 has helped control
90 (66) the disease.19–24 This initiative included both systematic
12 (8.8) examination of blood smears of asymptomatic people and
73 (54)
mass treatment of parasitemic individuals. This initiative
was initially successful; unfortunately, its success was not
108 (84.1)
sustained due to several factors including personnel and
91 (66.9)
53 (38.9) infrastructure disorganization, epidemiologic surveillance
11 (8.1) gaps and migrations associated with gathering activities
inherent to the Yanomami culture. Additionally, Yanomami
Indians tend to adhere poorly to malaria treatment. More
skilled personnel are needed and a specialized approach
should be taken by the health workers concerned with
malaria control in this reservation. The Indigenous Spe-
cial Health Districts, a network responsible for providing
medical attention to riverine and Indian communities in
the Rio Negro basin, was recently reorganized. This reor-
ganization may have been a strong contributing factor to
the increased malaria incidence rate in Santa Isabel do
Rio Negro, since it was accompanied by local and regional
politico-administrative disruptances and a halt in financial
support.
Malaria incidence has increased in the urban areas of
Amazonian Brazil,6,11 therefore, a major aim of the present
study was to characterize the distribution of malaria cases
within the urban/periurban districts of the studied munic-
ipality. To understand the most appropriate measures that
should be taken to control urban malaria, the vulnera-
bility of these areas to malaria and the ability of these
areas to sustain autochthonous transmission were assessed
by gathering demographic, environmental, and entomo-
logical data. A significant increase in the urban/periurban
APIs accompanied the increase of malaria incidence in
riverine and Indian villages. This increase was mostly due
to autochthonously transmitted cases; furthermore, these
cases were reported mainly in peripheral urban districts
linked by road to the urban zone. These roads pass through
many farms performing subsistence agriculture, and we
hypothesize that the daily movement of farmers along
these roads could maintain autochthonous urban transmis-
sion. Many water collection sites near these roads were also
identified as anopheline breeding sites.
Urban autochthonous malaria transmission is of special
concern because of its potential to introduce an epidemic
to a more populated setting. A significant increase in
the absolute number of malaria cases was also observed
in 2007. Once again, we argue that a lack of attention
to control measures such as the monitoring of potential
breeding sites, combined with an environment conducive
to malaria transmission, permitted the reemergence of this
disease. In addition, the vector species captured in the
urban area, An. darlingi, is highly anthropophilic and can
maintain malaria transmission even when present in low
 A.C. Cabral et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 556–562
density. We observed that the majority of the dwellings are
unsafe and contain openings through which mosquitoes
may freely penetrate. In addition, many of their inhabitants
do not know how malaria is transmitted or prevented. The
majority of breeding sites seen in the urban and periurban
areas are artificial water collection sites, which are byprod-
ucts of soil removal for road construction. The major urban
mosquito breeding site is located in a peripheral district
and was used until only recently as a clear water source,
since the Negro River water has an acidic pH and dark color.
Another main finding of this survey was the increase in
the proportion of cases caused by P. falciparum. The ratio
P.f./P.v. increased 5 times between 2006 and 2007. In the
Yanomami area the ratio P.f./P.v. reached 0.81 in 2007. This
also points to a failure in controlling transmission, since
early diagnosis and treatment reportedly have a greater
impact on malaria caused by P. falciparum than P. vivax.
Fluctuations in malaria incidence have been suggested
to correlate with El Niño Southern Oscillation (ENSO), the
periodic warming of the Pacific Ocean water that influences
the rainfall in many South American countries.25 How-
ever, the relationship between the ENSO index and malaria
incidence appears to be complex: ENSO-associated flood-
ing favors the occurrence of malaria epidemics in the dry
western coastal regions of South America, while droughts
enhance malaria transmission in Colombia.26 A similar
link between ENSO activity and malaria incidence was
observed in some African countries.27 However, Gagnon et
al.26 failed to detect a relationship between ENSO-related
climatic anomalies and malaria incidence fluctuation in
Brazil, and the ENSO index was moderate in 2002–2003
and low in 2004–2005 and 2006–2007. Although we did
not assess meteorological data in the studied area, our field
observations provided compelling evidence that factors
such as inadequate housing construction, artificial anophe-
line breeding sites and lack of attention to preventative
measures are more likely to be responsible for the increase
in malaria incidence than are climactic anomalies.
Finally, we propose that malaria transmission in
the studied municipality follows two distinct eco-
epidemiological patterns, each requiring a different control
approach. These two patterns are: (i) a stable pattern of
transmission in the Yanomami Indian reservation, a region
naturally containing mosquito breeding sites and there-
fore highly conducive to malaria transmission and (ii) an
unstable, epidemic pattern in the urban/periurban dis-
tricts, where artificial anopheline breeding sites combined
with inappropriately built settlements facilitate epidemics
and maintain autochthonous transmission. In both regions,
malaria incidence increased substantially in recent years.
The differences between the two patterns of malaria
transmission necessitate distinct control approaches.
Malaria transmission was successfully reduced on the
Yanomami Indian reservation by focusing on the detec-
tion of parasitemic individuals, including those without
symptoms, followed by mass treatment designed to stop
further transmission. In this area, little or no environ-
mental intervention can be carried out, since Yanomami
Indians are semi-nomadic and live in isolation in the for-
est. A similar eco-epidemiological pattern can probably be
extrapolated for many more non-Yanomami riverine com-
561
munities, and, by extension, similar control strategies are
probably appropriate for such communities. On the other
hand, urban/periurban malaria transmission should be
managed by intensive water monitoring of potential insect
breeding sites in and around the city, controlling adult stage
mosquitoes, and improving housing design. This strategy
is probably appropriate for controlling malaria transmis-
sion in other municipalities with similar demographic and
environmental characteristics.
Authors’ contributions: FAC-C and MNB conceived and
designed the study, analyzed and interpreted data, drafted
the manuscript and revised it critically for intellectual con-
tent; ACC, MSS-M and NFF performed epidemiological field
work, gathered and processed the secondary data, carried
out the entomological survey, analyzed and interpreted
data, performed the literature review, and revised criti-
cally the manuscript for intellectual content. FAC-C is the
guarantor of the paper.
Acknowledgements: We thank the students of the Post-
graduate Tropical Medicine Program at Instituto Oswaldo
Cruz/Fiocruz: Vinicius Martins de Menezes, Lucia Maria
Brum Soares, Daniela Martins Luciano, Gleicy Amorim
Macedo, Ricardo Tristão Sá, Vladimir Luna Tedesqui, and
Peliganga Luís Baião for essential support in field activi-
ties. We are grateful to the Brazilian Health Surveillance
Agency (SVS) officials for their technical assistance during
capture of mosquitoes and permission to access secondary
data and to Carla Dias of the Socio-Environmental Insti-
tute (ISA) for assistance on geographic localization of the
riverine communities.
Funding: The study on which this report is based was
supported with federal funds from the Brazilian Federal
Agency for Support and Evaluation of Graduate Education
(CAPES) and the National Council for Scientific and Tech-
nological Development (CNPq).
Conflicts of interest: None declared.
Ethical approval: This study was approved by the Evandro
Chagas Clinical Research Institute/Oswaldo Cruz Founda-
tion Research Ethics Committee.
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