Revista da Sociedade Brasileira de Medicina Tropical 45(4):425-429, Jul-Aug, 2012
1. Centro de Pesquisas Aggeu Magalhães, Fundação Oswaldo Cruz, Recife, PE. 2. Pós-Graduação em
Ciências Biológicas, Universidade Federal de Pernambuco, Recife, PE. 3. Departamento de Enfermagem,
Universidade de Pernambuco, Recife, PE.
Address to: Dra. Maria Edileuza Felinto de Brito. Depto. Imunologia/CPqAM/FIOCRUZ-PE.
Campus da UFPE, s/n, Cidade Universitária, 50670-420 Recife, PE, Brasil.
Phone/Fax: 55 81 2101-2641; 55 81 2101-2640
Received in 15/03/2012
Accepted in 20/06/2012
Cutaneous leishmaniasis in northeastern Brazil: a critical appraisal
of studies conducted in State of Pernambuco
Leishmaniose cutânea no nordeste do Brasil: uma avaliação crítica dos estudos realizados no
Estado de Pernambuco
Maria Edileuza Felinto de Brito1, 2, Maria Sandra Andrade3, Filipe Dantas-Torres1, Eduardo Henrique Gomes
Rodrigues1, Milena de Paiva Cavalcanti1, Alzira Maria Paiva de Almeida1 and Sinval Pinto Brandão-Filho1
Review Article/Artigo de Revisão
American cutaneous leishmaniasis (ACL) is a complex disease with clinical and epidemiological
features that may vary from region to region. In fact, at least seven different Leishmania species,
including Leishmania (Viannia) braziliensis, Leishmania (Viannia) guyanensis, Leishmania
(Viannia) lainsoni, Leishmania (Viannia) naiffi, Leishmania (Viannia) shawi, Leishmania
(Viannia) lindenbergi, and Leishmania (Leishmania) amazonensis, have been implicated in the
etiology of ACL in Brazil, and numerous phlebotomine sandfly species of the genus Lutzomyia
have been regarded as putative or proven vectors. Because ACL is a focal disease, understanding
the disease dynamics at the local level is essential for the implementation of more effective
control measures. The present paper is a narrative review about the ACL epidemiology
in Pernambuco, northeastern Brazil. Furthermore, the need for more effective diagnosis,
treatment, control and prevention strategies for the affected populations is highlighted. This
paper will provide researchers with a critical appraisal of ACL in Pernambuco. Hopefully, it
will also be helpful for public health authorities to improve current control strategies against
ACL at the state and country levels.
Keywords: Cutaneous leishmaniasis. Leishmania braziliensis. Reservoirs. Insect vectors.
A leishmaniose cutânea americana (LCA) é uma doença complexa com características
clínicas e epidemiológicas que podem variar de região para região. De fato, pelo menos, sete
diferentes espécies de Leishmania, incluindo Leishmania (Viannia) braziliensis, Leishmania
(Viannia) guyanensis, Leishmania (Viannia) lainsoni, Leishmania (Viannia) naiffi, Leishmania
(Viannia) shawi, Leishmania (Viannia) lindenbergi e Leishmania (Leishmania) amazonensis,
têm sido incriminadas na etiologia da LCA no Brasil, e numerosas espécies de flebotomíneos
do gênero Lutzomyia, foram considerados vetores suspeitos ou comprovados. Devido ao
seu caráter focal, a compreensão da dinâmica da LCA a nível local é imprescindível para
a implementação de medidas de controle eficazes. Este trabalho consiste de uma revisão
narrativa sobre a epidemiologia da LCA em Pernambuco, nordeste do Brasil. Além disso, se
enfatiza a necessidade de maior efetividade no diagnóstico, tratamento, controle e estratégias de
prevenção para as populações afetadas. Este artigo fornecerá aos pesquisadores uma avaliação
crítica da LCA em Pernambuco. Espera-se também contribuir com as autoridades de saúde
pública no aprimoramento das estratégias atuais de controle da LCA nos níveis estaduais e
Palavras-chaves: Leishmaniose cutânea. Leishmania braziliensis. Reservatórios. Insetos vetores.
American cutaneous leishmaniasis (ACL) is a
complex disease with clinical and epidemiological
features that may vary from region to region1.
Because ACL is a focal disease, understanding the
disease dynamics at the local level is essential for the
implementation of more effective control measures.
In Brazil, ACL presents variable epidemiological
patterns, which may vary according to the phlebotomine
sandfly species involved in transmission, population
susceptibility and the level of exposure as well as
the diversity and competence of reservoir hosts.
A number of studies on ACL in Pernambuco
State, northeastern Brazil, have been performed in
the past decades and have contributed enormously to
the knowledge of ACL ecoepidemiology at the state
and country levels2-7. In particular, the importance of
small terrestrial mammals in the transmission chain of
Leishmania (Viannia) braziliensis7, the most widespread
etiological agent of ACL in Brazil, has been demonstrated.
This paper is a narrative review regarding the
ACL epidemiology in Pernambuco. Articles were
searched in electronic databases (i.e., Medline,
Lilacs and SciELO) using the following search
terms: leishmaniasis, mucocutaneous leishmaniasis,
tegumentary leishmaniasis, Leishmania, Lutzomyia,
and Pernambuco. Search terms were used alone or
in combination and with no language or release date
restriction (as of January 2012). Studies investigating
the epidemiology, diagnosis, etiology, reservoirs
and vectors of ACL were included whereas those
exclusively focusing on visceral leishmaniasis were
excluded. Additionally, references of retrieved articles
were searched for relevant papers that could not have
been located in the searched databases. The importance
of control and prevention strategies for the affected
populations and the need for effective diagnostic tools
and treatment procedures are discussed. This paper
will provide researchers with a critical appraisal of ACL
in Pernambuco. Hopefully, it will also be helpful for
public health authorities to improve current control
strategies against ACL at the state and country levels.
Brito MEF et al - Critical appraisal of cutaneous leishmaniasis in northeastern Brazil
DIVERSITY OF ETIOLOGICAL AGENTS
Seven species of Leishmania have been implicated as ACL agents
in Brazil: Leishmania (Viannia) braziliensis, Leishmania (Viannia)
guyanensis, Leishmania (Viannia) lainsoni, Leishmania (Viannia) naiffi,
Leishmania (Viannia) shawi, Leishmania (Viannia) lindenberg, and
Leishmania (Leishmania) amazonensis8. However, L. (V.) braziliensis
is the main ACL etiological agent in Pernambuco and other Brazilian
In a study conducted in Amaraji and Cortes (two municipalities
from the southern Atlantic Forest region) (Figure 1) in 1991, two
strains isolated from humans and characterized with multilocus
enzyme electrophoresis (MLEE) exhibited an enzymatic profile
similar to L. (V.) braziliensis stricto sensu, except for the enzymes
isocitrate dehydrogenase-nicotinamide adenine dinucleotide
phosphate (IDH-NADP) and phosphoglucomutase (PMG), which
were different from the reference strain MHOM/BR/75/M2903.
These strains were grouped as a new zymodeme IOC-Z45, a variant
of the species12.
Between 1996 and 2000, in a longitudinal study conducted in
Raiz de Dentro, Refrigério and Tranquilidade from Amaraji, 30
strains were isolated from patients presenting predominantly single
ulcerated lesions. These strains were placed into serodeme 1 with
monoclonal antibodies. Through MLEE, they were all identified
as L. (V.) braziliensis, although some of them showed different
electrophoretic mobility profiles (electromorphs) for the PGM,
IDH-NADP and malic enzyme (ME) and were grouped into four
new zymodemes: IOC-Z72, IOC-Z73, IOC-Z74, and IOC-Z7510.
Another study in three different areas in Pernambuco
(Amaraji (southern Atlantic Forest), Paudalho (northern Atlantic
Forest region), and Moreno (metropolitan region of Recife)
(Figure 1) was performed in 2009. Sixty-seven samples isolated
from patients with different ACL clinical forms were identified as
L. (V.) braziliensis serodeme 1 with monoclonal antibodies. Through
MLEE, 10 different zymodemes (IOC-Z26, IOC-Z27, IOC-Z45,
FIGURE 1 - Diversity of Leishmania (Viannia) braziliensis zymodemes in three municipalities (Amaraji, Moreno and Paudalho) of Pernambuco. The geographic
regions mentioned (metropolitan region of Recife, Atlantic Forest region, scrub zone and semi-arid region) in the text are also depicted.
RMR: Região Metropolitana de Recife; ZM: Zona da Mata; A: Agreste; S: Sertão; SSF: Sertão do São Francisco.
IOC-Z72, IOC-Z73, IOC-Z74, IOC-Z75, IOC-Z78, IOC-Z105,
and IOC-Z106) were found (Figure 1). Most of these zymodemes
were classified9,10. It should be noted that this was the first report of
L. (V.) shawi in Pernambuco.
In a study performed in 2008 in Mundo Novo, a rural community
in São Vicente Férrer, a municipality of the Agreste region (scrub
region) (Figure 1) where visceral leishmaniasis has sporadically been
diagnosed in dogs and humans, 20 dogs were found to be positive
for L. (V.) braziliensis with polymerase chain reaction (PCR). This
finding revealed a high exposure level to Leishmania spp. in dogs in
this area11 and suggested that dogs might eventually be infected with
L. (V.) braziliensis.
These findings strongly indicate that the transmission cycle
complexity and the co-existence of two or more species circulating
in the same area may be reflected in the genetic polymorphism of this
Leishmania population. A recent study suggested that the parasite’s
genetic diversity may be associated with particular transmission
cycles, most likely reflecting the adaptation of different parasite clones
to distinct vector species12.
OCCURRENCE AND DISTRIBUTION OF VECTORS
During the 1940s, studies on phlebotomine sandflies in
northeastern Brazil reported the occurrence of Lutzomyia fischeri,
Lutzomyia evandroi, Lutzomyia squamiventris, and Lutzomyia
migonei in the Atlantic Forest region of Pernambuco13. Since then,
approximately 37 sandfly species have been identified in this state14.
From 1979-1980, a study was performed in Igarassu (northern
Atlantic Forest region), and Lutzomyia whitmani was the most
abundant species15. In another study conducted in Amaraji, one of
the major ACL foci in Pernambuco, eight species were identified, but
again, L. whitmani was predominant in domestic and peridomestic
areas. Furthermore, this sandfly was found to be naturally infected by
L. (V.) braziliensis4,16. Other studies have confirmed that L. whitmani
Rev Soc Bras Med Trop 45(4):425-429, Jul-Aug, 2012
is adapted to the domestic environment and can also be found
indoors in Amaraji16. Moreover, this species is highly anthropophilic17,
which partly explains the high prevalence of ACL in this area. A more
recent investigation in the municipality of Moreno also revealed the
predominance of L. whitmani6. Undoubtedly, L. whitmani is the most
important vector of L. (V.) braziliensis in Pernambuco.
A recent survey performed in São Vicente Férrer demonstrated
that in contrast with Igarassu and Amaraji, L. migonei was the
predominant species in domestic and peridomestic environments,
whereas Lutzomyia complexa and Lutzomyia sordelli were predominant
in forest remnants18. Similarly, a study conducted in a military training
area in Paudalho reported a high diversity of phlebotomine sandflies,
with the predominance of Lutzomyia complexa and Lutzomyia choti3,5.
In contrast, in a large study in an Atlantic Forest reserve located
in Recife, the most abundant species was Lutzomyia umbratilis19.
This sandfly is a vector of L. (V.) guyanensis, whose presence in
Pernambuco is uncertain.
The phlebotomine sandfly fauna of Pernambuco is rich. However,
L. whitmani is predominant in most of the ACL transmission foci,
mainly in domestic and peridomestic areas, whereas L. complexa or
other species prevail in wild environments5. Compared with other
northeastern Brazilian states, the phlebotomine sandfly fauna of
Pernambuco is more diverse than Alagoas, Ceará, Paraíba, Piauí,
Rio Grande do Norte, and Sergipe but not Maranhão and Bahia13.
The high abundance and widespread distribution of phlebotomine
sandfly vectors in Pernambuco indicate that most of the population
is exposed to Leishmania spp. infection.
wILD AND SYNANTHROPIC RESERVOIR HOSTS
Leishmania (V.) braziliensis has been detected in several wild and
synanthropic rodents of the genera Akodon20, Proechimys21, Rattus2,22,
Oryzomys2,23,24, Rhipidomys25, Nectomys and Necromys2 and marsupials
of the genus Didelphis2,21. In most cases, the isolates from these
animals have neither been properly identified nor characterized; the
identification was typically based on morphological characteristics
and the behavior of the parasites in culture only.
A pioneering study targeting small mammals as probable
Leishmania (V.) braziliensis reservoirs in Pernambuco was conducted
in Amaraji, and a total of 407 rodents and 71 marsupials were trapped
and analyzed. Remarkably, amastigotes in liver and spleen imprints
consistent with Leishmania spp. were found in specimens of Nectomys
squamipes (n=5), Necromys (syn. Bolomys) lasiurus (n=5), and
Rattus rattus2. Another study in the same area presented evidence of
Leishmania infection in several rodent species. Five L. (V.) braziliensis
isolates from N. lasiurus and one from R. rattus were identified
and characterized, and different zymodemes were identified7. It
is noteworthy that the zymodeme IOC-Z74 was isolated from
human patient samples, sentinel hamsters, vectors and both wild
and synanthropic rodents, suggesting that this is the predominant
zymodeme in the region7,10. Considering the difficulties related to the
cultivation, isolation and maintenance of L. (V.) braziliensis parasites,
these results represented an important achievement26. Similarly, a
study in São Vicente Férrer also provided evidence of Leishmania
infection in N. squamipes, R. rattus, and Holochilus sciureus27 with PCR.
Usually, these animals display no visible lesions consistent
with ACL despite being parasitized, suggesting that the Leishmania
parasites in their primitive form have adapted to these hosts22.
Therefore, these animals have the potential to act as long-term
maintainers of L. (V.) braziliensis in nature7. The identification of
N. squamipes, N. lasiurus and R. rattus hosting L. (V.) braziliensis
represents a major contribution to the knowledge of the epidemiology
of ACL in Brazil and allows for a better understanding of the role of
these species as reservoirs of this important parasite7.
Although serological and/or molecular evidence of Leishmania
(V.) braziliensis in domestic dogs from ACL endemic areas have been
reported2,11, further research is necessary to ascertain the role of these
animals in the ACL transmission chain in Pernambuco.
AMERICAN CUTANEOUS LEISHMANIASIS IN HUMAN
From a historical perspective, the first ACL cases recorded in
Pernambuco date back to the 1930s, when the disease was detected
in rural workers from the Atlantic Forest region28,29.
From 1989 to 1991, 1.604 cases were reported to the Ministério
da Saúde (MS), most (64.2%) of which were detected in the Atlantic
Forest region2, particularly in the municipalities of Amaraji and
Cortês. In the beginning of the 1990s, an active search for ACL cases
in this area identified 127 human cases2. Subsequent studies showed a
10-fold increase in ACL over a 10-year period in the region4. From an
epidemiological standpoint, the infection was more prevalent in adult
males (but was also recorded in females) and children, eventually
affecting all of the members of the same family4.
In 1996, an outbreak of ACL occurred in a military training
camp (Campo de Instrução Marechal Newton Cavalcanti - CIMNC,
Paudalho) in a region of somewhat preserved Atlantic Forest,
affecting 26 trainee soldiers. An epidemiological investigation in
this area detected a 24.1% infection prevalence in that population3.
From 1996 to 2010, 197 ACL cases were diagnosed among trainee
soldiers from CIMNC; an average of 16 cases per year. Therefore, it
was concluded that a primary enzootic cycle was established in this
area with a somewhat defined fluctuation of cases, with sporadic
outbreaks followed by low-occurrence periods5,30.
In 2010, 25 ACL cases were registered in an outbreak in Igarassu,
and an active search detected 49 additional cases in the region31.
The diagnosis was mostly based on the presence of skin lesions in
conjunction with the microscopic detection of amastigotes in skin
samples and/or a positive Montenegro skin test. Most patients presented
with typical localized lesions. Different age classes (>10 years) and
both sexes were affected, although most of the patients were males31.
Using the Montenegro skin test, a study conducted in Moreno
reported a 30% positivity in a population of 481 individuals. The
positivity was higher among males and among individuals aged
11 to 30 years. Interestingly, 67% of the positive individuals had
no previous ACL history6.
From 2001 to 2010, 4.855 ACL cases were recorded in Pernambuco,
with an average of 485 cases per year32. In fact, ACL is endemic in
all of the geographical regions of Pernambuco, and outbreaks are
sporadically detected in the Agreste and Atlantic Forest regions4.
Although the highest prevalence of ACL is still recorded in the
Atlantic Forest region7, the disease is spreading to other areas, and
the incidence is increasing in the entire state. Importantly, most of the
affected people live in poor villages in rural areas and are permanently
exposed to the disease risk factors, typically for occupational reasons,
as observed in other Brazilian regions33.
The authors declare that there is no conflict of interest.
CONFLICT OF INTEREST
AMERICAN CUTANEOUS LEISHMANIASIS DIAGNOSIS
The routine diagnosis of ACL in Pernambuco, particularly
in rural areas, is based on clinical and epidemiological criteria.
In Recife, the state’s capital, both traditional (e.g., cytology) and
modern techniques (e.g., PCR) are available in reference hospitals
and research centers.
A study performed in 2000 on the antibody response of patients
from an endemic ACL area with immunoblotting using antigenic L.
(V.) braziliensis fractions identified the 27 and/or 30 kDa soluble
antigens, which were considered promising for ACL diagnosis34.
Immunoblotting was more sensitive (91%) and specific (100%)
than the indirect immunofluorescence antibody test (IFAT) and
enzyme-linked immunosorbent assay (ELISA). In 2001, the same
antigenic fractions were employed to analyze the antibody response
level in patients before and after treatment35. Because the levels of
these antigens were decreased approximately twofold in clinically
recovered patients, it was concluded that they may be used as markers
of healing or parasite persistence in human patients.
The introduction of molecular biology techniques has greatly
improved the diagnosis of ACL in Pernambuco and elsewhere
in Brazil. Two specific systems for the subgenera Viannia and
Leishmania have been assessed, revealing 95.5% and 88.2% sensitivity,
respectively, and 100% specificity for healthy individual samples36.
Indeed, PCR-based methods are significantly more sensitive than
the conventional tests, such as direct examination, histopathological
examination and skin sample culture.
Polymerase chain reaction, culture and histopathological
examination were also compared in 32 samples from clinically
cured ACL patients after chemotherapy. Leishmania (Viannia)
sp. Deoxyribonucleic acid (DNA) was detected in 93.7% of the
patients, and three strains were identified through culture. In the
histopathological examination, no parasite was found. However,
fibroblastic changes were present in all of the cases, with an
inflammatory focus observed in four cases, suggesting the persistence
of parasites in these patients after chemotherapy37. This result was
confirmed by the parasite isolation from (n=3) individuals’ scars
5 years after clinical cure37.
In a study involving 19 patients with lesions compatible with
ACL from different localities of Pernambuco, 89% of them were
positive with the Montenegro skin test, 79% with IFAT, 58% with
skin cytology and 75% with PCR38. These results clearly illustrate the
importance of combining different diagnostic techniques to improve
the detection level.
FINAL COMMENTS AND CONCLUSIONS
Many ecoepidemiological aspects of ACL in Pernambuco have
been characterized in recent years as an important contribution to
the understanding of the infection prevalence and disease expression.
Moreover, the characterization of vectors and reservoir hosts involved
in the transmission and maintenance of L. (V.) braziliensis in this
region has also been assessed.
Leishmania (V.) braziliensis is the main etiological agent of ACL
in Pernambuco, where 10 or more variants circulate. Phlebotomine
sandfly vectors are widely distributed over the state’s territory, with
the predominance of L. whitmani in domestic and peridomestic areas
and L. complexa in forest remnants in most ACL foci. Concerning
L. (V.) braziliensis reservoirs, N. squamipes, N. lasiurus and R. rattus
have been suggested as possible parasite maintainers in natural
transmission cycles, but further transmission studies are needed to
better understand their role. For instance, R. rattus, originally from
Europe, established as synanthropic animals throughout Brazil and
now it can be found both in human dwellings and in the fields. On
the other hand, from an evolutionary viewpoint, its relationship with
L. (V.) braziliensis is recent and it is unknown to what extent this
imported rodent has adapted to this native parasite and vice versa.
The Atlantic Forest region is responsible for more than 60% of
all of the ACL cases reported in Pernambuco, which emphasizes the
need to establish and strengthen preventive and control measures
against the disease in this region. Nonetheless, it is also important
to promote continuous education for physicians and the capacity of
public health professionals working in newly detected ACL foci to
speed diagnostic and treatment procedures in these areas.
The diversity of Leishmania species or variants found in vertebrate
hosts and vectors reflects the complexity of ACL in Pernambuco,
which makes the design and implementation of control programs
for this endemic disease a challenge for public health authorities.
It is expected that this paper will provide public health authorities
with essential information on ACL in this Brazilian state, which may
be helpful for designing more effective control programs. Current
control strategies have not been sufficient to stop or even reduce
the disease burden.
Thanks to José Ferreira Marinho-Junior for his technical
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