Revista da Sociedade Brasileira de Medicina Tropical 46(1):60-66, Jan-Feb, 2013
Epidemiological aspects of American cutaneous
leishmaniasis and phlebotomine sandfly population, in the
municipality of Monte Negro, State of Rondônia, Brazil
Address to: Dra. Carolina Bioni Garcia Teles. Depto. Medicina/Faculdade
São Lucas. Rua Alexandre Guimarães 1927, Bairro Areal, 78915-620
Porto Velho, RO, Brasil.
Phone: 55 69 3211-8000; Fax: 55 69 3211-8019
Received in 05/04/2012
Accepted in 22/06/2012
Carolina Bioni Garcia Teles, Sergio Almeida Basano, Marcelo Zagonel-Oliveira,
Jimmy Joy Campos, Arley Faria José de Oliveira, Rui Alves de Freitas,
Jansen Fernandes Medeiros, Felipe Arley Costa Pessoa, Aldina Barral
and Luís Marcelo Aranha Camargo
. Departamento de Medicina, Faculdade São Lucas, Porto Velho, RO. . Departamento de Genética, Universidade Federal do Rio Grande do Sul, Porto Alegre,
RS. . Curso de Medicina, Universidade Federal do Acre, Rio Branco, AC. . Programa de Pós-Graduação em Diversidade Biológica, Universidade Federal do
Amazonas, Manaus, AM. . Laboratório de Leishmaniose e Doença de Chagas, Instituto Nacional de Pesquisas da Amazônia, Manaus, AM. . Coordenação
Sociedade, Ambiente e Saúde, Instituto Nacional de Pesquisas da Amazônia, Manaus, AM. . Grupo de Pesquisa em Ecologia de Doenças Transmissíveis na
Amazônia, Instituto Leônidas e Maria Deane, Fundação Oswaldo Cruz, Manaus, AM. . Centro de Pesquisas Gonçalo Muniz, Fundação Oswaldo Cruz, Salvador,
BA. . Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, Monte Negro, RO.
Introduction: This work was carried out on the purpose of identifying the species of phlebotomine sandflies in the municipality
of Monte Negro, state of Rondonia, Brazil, that may have been transmitting the American cutaneous leishmaniasis (ACL), and
concisely describe epidemiological aspects of disease. Methods: The epidemiologic and socioeconomical indicators were obtained
from government institutions and the local Municipal Secretary of Health. Phlebotomine sandflies were captured using CDC light
traps between July 2006 to July 2008. The total of 1,240 of female sandflies were examined by PCR method directed to k-DNA.
Results: There has been a significant decrease in the incidence of ACL of about 50% over the last ten years in the municipality.
A total of 1,935 specimens of 53 sandfly species were captured, three of the genus Brumptomyia genus and 50 of the genus
Lutzomyia. The predominant species was Lutzomyia acanthopharynx, Lutzomyia whitmani, Lutzomyia geniculata and Lutzomyia
davisi. None were positive for Leishmania sp. Conclusions: Four sandflies species were found in the State of Rondonia for the
first time: Brumptomyia brumpti, Lutzomyia tarapacaensis, Lutzomyia melloi and Lutzomyia lenti. The presence of Lutzomyia
longipalpis, was also captured. Socioeconomical improvement of Brazilian economy and the increase of environmental surveillance in the
last 15 years collaborated in the decrease of people exposed to vectors, reducing the incidence of ACL.
Keywords: Phlebotomine sandflies. Epidemiology. Leishmaniasis. Amazon.
In the Americas, Leishmania is transmitted by the females of
some species of phlebotomine sandflies of the genus Lutzomyia.
According to Rangel & Lainson1, over than 400 Lutzomyia
species have been found in Brazil, 122 found in the Amazonian
region, out of which 25 were found to have an anthropophlic
One-hundred and six (106) species of Lutzomyia and
three species of Brumptomyia were recorded in the State of
Rondônia2-4. According to Shaw et al.5, the most prevalent
Leishmania species found in humans in the State of Rondônia
are Leishmania (Viannia) braziliensis, L. (V.) lainsoni and L. (V.)
guyanensis. In 2010, 922 occurrences of American cutaneous
leishmaniasis (ACL) were recorded in the State of Rondônia6,
and such an incidence has been gradually decreasing over the
last 10 years. Analysis of the ACL transmission circumstances
in each area is complex due to the diversity of species of
the etiologic agents, vectors and reservoirs involved in the
transmission cycle, which has been a challenge for the healthcare
system regarding both the diagnosis and treatment due to the
broad spectrum of lesions, operational difficulties for diagnosis
and chemotherapy toxicity.
One of the challenges regarding the ACL control and
diagnosis is the lack of knowledge about the epidemiologic
conditions, specially the study on the distribution of the
phlebotomine sandflies population, the frequency and the
characterization of its species, although some studies have
already been carried out on the occurrence of phlebotomine
sandflies and ACL in the State of Rondônia3,4,7,8.
Nevertheless, some areas remain unexplored while others
have been in geo-economic transformation process, and required
further study in order to identify the phlebotomine species that
account for the occurrence of ACL. Such study was carried
out with forest sections nearby the dwellings around the rural
area of the municipality of Monte Negro in Rondônia, an ACL
Teles CBG et al - Leishmaniasis in the municipality of Monte Negro/Rondônia
FIGURE 1 - Map of Brazil highlighting the State of Rondônia, Brazil, and the localization of the municipality of Monte Negro, in the West Amazon and the nine cases of
American cutaneous leishmaniasis (ACL) registered during the study in 2006.
RO: State of Rondônia.
Study area and population
The study area is situated in the Brazilian Western Amazon,
in the municipality of Monte Negro (Figure 1), located at 250km
southwest of the City of Porto Velho (capitol), central region
of the State of Rondônia, between 10o15’S and 63o17’W. The
weather is characterized by two well marked seasons, one dry
and the other humid, with a mean annual precipitation up to
2,020mm, and mean temperature of 25.8ºC9. A population of
14,204 inhabitants occupying an area of 1,413.4km2 has been
estimated out of which 60% live in the rural area. Its economy is
based on agriculture (coffee, corn, and rice), cattle farming (beef
and dairy cattle), and wood harvest exploitation and processing10.
Epidemiologic data collection
The data were obtained from the Ministry of Health of
Brazil11 for the period between 1990 and 2010 for Brazil,
Rondônia and Monte Negro, and the data regarding the nine
autochthonous cases in Monte Negro were reported by the
Secretary of Health of Monte Negro in 2006.
Environmental, economic and demographic indicators
were obtained from government institutions, namely Brazil's
National Institute for Space Research (INPE), Institute for
Applied Economic Research (IPEA) and Brazilian Institute of
Geography and Statistics (IBGE).
Phlebotomine sandfly capture
The phlebotomine sandflies were captured between July
2006 to July 2008 in residual woods located nearly 30 to 50m
from the dwellings in nine human cases of ACL out of a total
of 20 cases reported within the period to the Secretary of Health
of Monte Negro (Figure 1). Three visits were made at each site
(27 visits in the total). As there were used 2 or 3 Centers for Disease
Control (CDC) light traps from 6AM to 6PM per capture, a total
of 81 captures were realized. The phlebotomine sandflies were
identified according to the entomologic keys of Young & Duncan12.
19901991 199219931994 19951996 199719981999 2000 200120022003 200420052006200720082009 2010
FIGURE 2 - Incidence of American cutaneous leishmaniasis in the municipality of Monte Negro,
State of Rondônia, Brazil, between 1990 and 2010 (occurrences per 100 thousand inhabitants).
Source: Sistema de Informação de Agravos de Notificação (SINAN), 2011.
Rev Soc Bras Med Trop 46(1):60-66, Jan-Feb, 2013
Extraction of DNA from captured females of
Female sandflies were initially sorted by species, and date and
place of capture, and were then grouped into 2 to 20 specimens
in micro test tubes for deoxyribonucleic acid (DNA) extraction
based on the method adapted by Mukhopadhyay et al.13. Twenty
microliters of buffer was added in the micro test tubes containing
groups up to 10 specimens, and 35µL of buffer in the tubes
containing over 10 specimens. They were heated for 10min up
to 95°C in water bath (bain-marie), and then the insects were
macerated by using a homogenizer, added with buffer STE (NaCl
0.1M, Tris-HCl 10mM pH 8.0 e EDTA. 1mM) until completing
a volume of 50µL. Next, they were again heated in water bath
(37oC) up to 95°C for 10min, and then centrifuged at 12,000rpm
for 2min. About 20µL of supernatant (DNA) was then transferred
to another tube. After the extraction they were stored at 20º C for
polymerized chain reaction (PCR).
Detection of natural infection phlebotomine sandfly by
The amplification for the genus Leishmania was based
on the PCR method directed to the conserved region of the
kinetoplast DNA (kDNA) minicircles among all the species
of Leishmania sp., and performed with primers 5’-GGG(GT)
AGGGGCGTTCT(G/C)CGAA-3’ and 5’-(G/C)(G/C)(G/C)
(A/T)CTAT(A/T)TTACACCAACCCC3’14; the product
obtained was 120pb. The total volume was 50µL divided
into 4µL of the DNA of the samples and 46µL of a mixture
compounded by 37.25µL of sterile milli-Q water, 5µL of 10X
taq buffer, 1.5µL of MgCl2, 1µL of dNTPs (10 mM), 0.75µL of
primer 1 (10µM), 0.75µL of primer 2 (10µM) and 0.5 of Taq
The amplification was processed by an automatic thermal
cycler using the following cycle: initial denaturation at 95ºC for
5min, followed by 40 repetitions of denaturation at 94ºC for
30 seconds, annealing at 55ºC for 30sec, and extension at 72ºC
for 1min and 30sec. The final extension was at 72ºC for 10min.
The products amplified by PCR were analyzed by agarose
gel electrophoresis 2% stained in ethidium bromide solution and
examined by exposure to ultraviolet light (UV). For negative
control, male phlebotomine sandfly DNA was used, while for
positive control the sandfly DNA was used added to 200µL of
a culture of Leishmania amazonensis strain IFLA/BR/67/PH8.
One thousand nine hundred and thirty five phlebotomine
sandflies were captured: 695 males (36%) and 1,240 females
(64%) (Table1 and Table2). A total of 53 species were
identified: three of the genus Brumptomyia (32 samples -
1.6%) and 50 of the genus Lutzomyia (1,903 samples - 98.4%).
The specimens of the genus Lutzomyia were sorted into the
following subgenus: L. (Evandromyia) (15), L. (Lutzomyia) (23),
L. (Micropygomyia) (5), L. (Nyssomyia) (321), L. (Pressatia) (8),
Psathyromyia (60), L. (Psychodopygus) (379), L. (Sciopemyia)
(68), L. (Trichophoromyia) (76), L. (Viannamyia) (14); and into the
following groups (Table 2): Aragaoi Group (9), Migonei Group
(98), Oswaldoi Group (103), Saulensis Group (44), Verrucarum
Group (29) and more 651 samples of a ungrouped species
Among the 53 species captured, some were reported in
the State of Rondônia for the first time: B. brumpti (0.4),
L. tarapacaensis (0.7%), L. melloi (0.05%) and L. lenti
(0.05%). The most abundant species found in this survey
were L. acanthopharynx (651 samples - 33.6% out of the total
collected), L. whitmani (180 samples - 9.3%), L. geniculata
(155 samples - 8%) and L. davisi (151 samples - 7.8%), which
represent 58.7% of the total.
Other phlebotomine sandfly species, of ACL vectors were
captured in Monte Negro such as L. flaviscutellata, L. umbiquitalis,
L. complexa and L. carrerai. L. longipalpis, the visceral
leishmaniasis (VL) vector in Brazil, was also captured.
For natural infection analysis, a PCR was performed with all
females phlebotomine sandflies collected. However, no sample
has been found to be positive for Leishmania sp.
Since 1990, SINAN6 has been reporting a gradual decrease by
53% in the ACL incidence in Monte Negro, a decrease of 43% in
Rondônia, while, in Brazil, it has been noticed a decrease rate of
about 31%. The reduction of the number of cases after 1990, as
shown in Figure 2, reported by the Brazilian Ministry of Health
sets a consistent decrement pattern.
Nine human cases were followed up in this study, all them from
the rural zone, and the most affected group was represented by men
(98%) between 15 and 50 years old, who lived in little settlements
around the urban area of Monte Negro.
According to National Institute for Space Research (INPE)16,
between 2004 and 2010 there was a reduction in deflorestation,
from 27,772km2/year to 7,646km2/year.
The economic results also must be looked upon. Between 2004 and
2009 there was an increase by 18% in the number of families benefitted
Teles CBG et al - Leishmaniasis in the municipality of Monte Negro/Rondônia
TABLE 1 - Phlebotomine sandfly population of the genus Brumptomyia and subgenera Lutzomyia was captured using CDC light traps in Monte Negro, State of Rondônia,
Brazil, between July 2006 to July 2008.
Genus Subgenera Species Males Females Total Percentage
Brumptomyia B. brumpti* 9 - 9 0.46
B. pentacantha 3 - 3 0.15
B. sp. - 20 20 1.03
Lutzomyia (Evandromyia) L. tarapacaensis* 2 11 13 0.70
L. monstruosa 0 2 2 0.10
(Lutzomyia) L. evangelistai - 3 3 0.15
L. longipalpis 6 - 6 0.31
L. sherlocki 2 12 14 0.72
(Micropygomyia) L. micropyga 3 2 5 0.25
(Nyssomyia) L. antunesi 24 71 95 4.90
L. flaviscutellata 16 26 42 2.20
L. shawi - 3 3 0.15
L. umbratilis 1 - 1 0.05
L. whitmani 60 120 180 9.30
(Pressatia) L. triacantha 4 4 8 0.41
(Psathyromyia) L. campbelli 1 1 2 0.10
L. dendrophyla 8 13 21 1.08
L. lutziana 16 16 32 1.65
L. punctigeniculata 1 - 1 0.05
L. shannoni 3 1 4 0.21
(Psychodopygus) L. amazonensis - 5 5 0.26
L. carrerai ** 1 1 2 0.10
L. claustrei 2 9 11 0.60
L. complexa 2 3 5 0.25
L. davisi 51 100 151 7.78
L. geniculata 26 129 155 8.01
L. hirsuta ** 16 26 42 2.20
L. lainsoni 1 7 8 0.41
(Sciopemyia) L. servulolimai 8 20 28 1.44
L. sordellii 13 27 40 2.06
(Trichophoromyia) L. auraensis 22 - 22 1.13
L. clitella 9 - 9 0.46
L. melloi* 1 - 1 0.05
L. octavioi 5 - 5 0.25
L. ubiquitalis 8 3 11 0.60
L. sp. - 28 28 1.44
(Viannamyia) L. furcata 6 8 14 0.72
Total 334 709 1,043 54.0
B: Brumptomyia; L: Lutzomyia; CDC: Centers for Disease Control. *The first time for Rondônia; **Taxons renamed as species by Carvalho GML et al. Mem Inst Oswaldo Cruz 2006; 10:129-136. The
relative abundance of each species collected in the study area expressed as a percentage of the total of 1935 of sandflies collected.
Rev Soc Bras Med Trop 46(1):60-66, Jan-Feb, 2013
by the “Family Allowance Program”(Bolsa-Família) in the North
Region, and the increase in the formal employment rate in the main
Brazilian metropolitan areas by 24.4% between 2002 and 2010 (Source:
www.ipeadata.gov.br on Dec 28, 2011)17. On the other hand, the
migratory tendency to the North Region, resulted in a negative balance
of less 35,159 people between 2004 and 200910,17.
From all 53 species captured, four were new records for the
State of Rondônia: B. brumpti, L. tarapacaensis, L. melloi and
L. lenti. The surveys carried out in the State of Rondônia2-4, and the
new reports of phlebotomine species made by this work totalize
110 species of Lutzomyia and 4 Brumptomyia for Rondônia.
In the present study L. acanthopharynx, L. whitmani,
L. geniculata and L. davisi together represented 58.7% of
all the sandflies caught. According to Gil et al.3,4, the species
L. davisi and L. whitmani were the most abundant, and were
the vectors closely associated with ACL transmission around
the region, along with other predominant species such as
L. umbratilis, L. llanosmartinsi, L. dendrophyla, L. nevesi,
P. carrerai and P. hirsutus.
The species L. whitmani and L. davisi have proved to be
significant vectors of Leishmania that cause ACL either in the
enzootic cycle and in the peridomestic cycle3,18. The prevalence
of these vectors suggests the possibility of transmission
in the peridomestic environment. The confirmation of the
previous studies has associated L. davisi with the transmission
of Leishmania (Viannia) naiffi3 and Leishmania (Viannia)
braziliensis18 in the State of Rondônia. Gil et al.3 complement
that the high number of L. davisi captured in Shannon-type traps
reflects its anthropophilic habit, while Azevedo et al.19 reports
that the high L. whitmani density may be associated with the
changes in the original vegetation and the better adaptation to
new environmental conditions.
Many studies have shown the vectorial potential of
L. whitmani in the natural anthropic environments regarding the
transmission of Leishmania (Viannia) braziliensis, L. (V.) shawi
and L. (V.) guyanensis in some states of Northeast, Southeast,
South, West Central and Amazonian region1,20-23.
In the areas studied other vectors of ACL were identified,
such as L. flaviscutellata, the main vector of Leishmania
(Leishmania) amazonensis, which has been also found to be
parasitized by Leishmania (Viannia) guyanensis in the French
Guiana24; L. umbiquitalis, the vector of Leishmania (Viannia)
lainsoni in Brazil25; L. complexa, species considered to be a
Leishmania (Viannia) braziliensis vector26; Leishmania carrerai
is considered to be a Leishmania (Viannia) braziliensis vector
according to Grimaldi et al.27, who has characterized the parasite
in phlebotomine sandflies as naturally infected in the Brazilian
In addition to the ACL vectors, L. longipalpis, the VL
vector in Brazil, was collected in the region. Although the
incidence of VL in Rondônia has been exclusively associated
with allocthonous cases (0.07 per 100 thousand inhabitants)28,
the presence of L. longipalpis should be a factor of concern
as, in the Amazon region, VL is already autochthonous in the
States of Pará, Roraima, and Tocantins22,29,30 and areas of the
Southeast of Brazil, that were not traditional endemic areas of
VL, had registered several autochthonous cases over the last ten
years22,30,31. On the other hand, according to serologic studies
TABLE 2 - Sand flies groups of Lutzomyia captured in Monte Negro, State of Rondônia, Brazil, from July 2006 to July 2008 with CDC light traps.
Genus Group Species Males Females Total Percentage
Lutzomyia Aragaoi L. abunaensis 2 - 2 0.10
L. aragaoi 3 1 4 0.20
L. barretoi barretoi 2 - 2 0.10
L. coutinhoi 1 - 1 0.05
Migonei L. bacula 23 52 75 3.87
L. lenti* 1 - 1 0.05
L. termitophila 0 5 5 0.25
L. walkeri 6 10 16 0.82
L. williamsi 1 - 1 0.05
Oswaldoi L. goiana 60 43 103 5.32
L. wilsoni 2 - 2 0.10
Verrucarum L. nevesi 6 12 18 0.93
L. serrana 6 5 11 0.60
Ungrouped species L. acanthopharynx 248 403 651 33.64
Total 361 531 892 46.0
L: Lutzomyia; CDC: Centers for Disease Control. *The first time for Rondônia; **Taxons renamed as species by Carvalho GML et al. Mem Inst Oswaldo Cruz 2006; 10:129-136. The relative abundance
of each species collected in the study area expressed as a percentage of the total of 1935 of sandflies collected.
Teles CBG et al - Leishmaniasis in the municipality of Monte Negro/Rondônia
The authors declare that there is no conflict of interest.
CONFLICT OF INTEREST
We are in debt to Prof. Marisis Camargo and Prof. Ricardo
Ferreira for the English review and critical suggestions for the
1. Rangel EF, Lainson R. Flebotomíneos do Brasil. Rio de Janeiro: FIOCRUZ;
2. Aguiar GM, Medeiros WM. Distribuição regional e hábitats das espécies de
flebotomíneos do Brasil. In: Rangel EF, Lainson R, editors. Flebotomíneos do
Brasil. Rio de Janeiro: FIOCRUZ; 2003. p. 207-255.
3. Gil LHS, Basano SA, Souza AA, Silva MGS, Barata I, Ishikawa ED, et al.
Recent observations on the sandfly (Diptera: Psychodidae) fauna of the State
of Rondônia, western Amazônia, Brazil: the importance of Psychdopygus
davisi as a vector of zoonotic cutaneous leishmaniasis. Mem Inst Oswaldo
Cruz 2003; 98:751-755.
4. Gil LHS, Araújo MS, Villalobos JM, Camargo LMA, Ozaki LS, Fontes CJF,
et al. Species structure of sandfly (Diptera: Psychodidae) fauna in the Brazilian
western. Rio de Janeiro: Mem Inst Oswaldo Cruz 2009; 104:955-959.
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of Monte Negro, Rondônia State, western Amazonia, Brazil. Ann Trop Med
Parasitol 2007; 101: 681-688.
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complex in southern Amazonas and Rondônia, Brazil (Diptera: Psychodidae).
Mem Inst Oswaldo Cruz 1989; 84:363-369.
8. Aguiar DM, Oliveira TMFS, Cavalcante GT, Labruna MB, Camargo LMA,
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12. Young DG, Duncan MA. Guide to the identification and geographic distribution
of Lutzomyia sandflies in Mexico, the West Indies, Central and South America
(Diptera: Psychodidae). Mem Amer Entomol Inst 1994; 54:1-881.
13. Mukhopadhyay J, Ghosh K, Braig HR. Identification of cutaneous leishmaniasis
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polymorphic DNA. Acta Tropica 2000; 76:277-283.
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et al. Polymerase chain reaction (PCR) is highy sensitive for diagnosis of mucosal
leishmaniasis. Acta Tropica 2005; 94:55-59.
15. Marques MJ, Volpini AC, Genaro O, Mayrink W, Romanha AJ. Simple form
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e regionais [Internet]. Brasília: Presidência da República; [Cited 2011 January
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Characterization and classification of leishmanial parasites from humans, wild
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performed in Monte Negro8, infected dogs and phlebotomine
sandflies are in contact as dogs were found to be serologically
positive for Leishmania.
The knowledge of the phlebotomine sandfly fauna in
Rondônia remains still insufficient, while the last surveys
regarding the phlebotomine sandfly population has reported
new occurrences of its species3,4.
Although 64% of the phlebotomine sandflies collected were
females, the natural infection analysis for PCR was negative
for Leishmania sp. In endemic leishmaniasis areas, the rates of
natural infection by Leishmania in phlebotomine sandflies have
been historically low32,33. Soares et al.34 explain the low infection
rate due to ecologic relations such as the habitat pattern, the
intraspecific behavior, the vector feeding cycle, the genetic
endowment and immunity of the population of reservoirs of
The epidemiologic data points to a significant decrease in the
incidence a ACL of about 53% and 43% over the last ten years in
Monte Negro and Rondônia and 31% in Brazil. The municipality
of Monte Negro is an historical area of transmission of ACL
that accounted for a incidence of 59 cases/100,000 inhabitants
in 2010. The nine humans cases followed up in this study was
represented for mens between 15 and 50 years old, which is
the most susceptible age group, reported by some authors35-37.
The nature of the zoonotic transmission becomes evident when
it is noticed that 80% of the patients were engaged in activities
associated with the permanence in the forest (hunting, fishing,
lumbering), although 20% had not such activities, suggesting
peridomestic transmission. Murback et al.38, which suggested
that the ACL transmission in man in the productive age bracket
are likely to be higher due to the fact that they leave their
domiciliary environment for work or leisure, and are then more
exposed to the timberland areas.
The economical and environmental surveillance improvement
in Brazil in the last 15 years imply in a reduction of the
self-employed labor availability for risky activities connected
to the likeliness of ACL occurrences such as lumbering, gold
digging and clandestine land occupation. Such background may
have led to a decrease in the insertion of collectors and hunters
inside the woods that has reduced the likeliness of contamination
by the ACL vectors, and had a positive impact in the incidence
of the disease.
Nevertheless, in spite of the economic advancements, the
social development, and better environmental surveillance,
ACL appears as a permanent residual focal point in the region.
19. Azevedo ACR, Souza NA, Meneses CR, Costa WA, Costa SM, Lima JB, et al.
Ecology of sandflies (Diptera: Psychodidae: Phlebotominae) in the North of the
state of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz 2002; 97:459-464.
20. Mayrink P, Williams MV, Coelho M, Dias A, Vianna Martins, PA, Magalhães CA,
et al. Epidemiology of dermal leishmaniasis in the Rio Doce Valley, State of
Minas Gerais, Brazil. Ann Trop Med Parasitol 1997; 73:123-137.
21. Freitas RA, Naiff RD, Barrett TV. Species diversity and flagellate infections
in the sandfly fauna near Porto Grande, State of Amapá, Brazil (Diptera:
Psychodidae. Kinetoplastida: Trypanosomatidae) Mem Inst Oswaldo Cruz
22. Rangel EF, Vilela ML. Lutzomyia longipalpis (Diptera, Psychodidae,
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