Content uploaded by Dennis R A Mans
Author content
All content in this area was uploaded by Dennis R A Mans on Apr 18, 2017
Content may be subject to copyright.
Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname
Dennis RA Mans1*, Alida D Kent2, Ricardo VPF Hu3 and Henk DFH Schallig4
1Department of Pharmacology, Faculty of Medical Sciences, Anton de Kom University of Suriname, Paramaribo, Suriname
2Department of Parasitology, Faculty of Medical Sciences, Anton de Kom University of Suriname, Paramaribo, Suriname
3Dermatology Service, Ministry of Health, Paramaribo, Suriname
4Department of Medical Microbiology, Academic Medical Centre, Amsterdam, The Netherlands
*Corresponding author: Dennis RA Mans, Department of Pharmacology, Faculty of Medical Sciences, Anton de Kom University of Suriname, Kernkampweg 5-7,
Paramaribo, Suriname, Tel: +597-441071; Fax: Fax: 597-441071; E-mail: dennis_mans@yahoo.com, dennis.mans@uvs.edu
Received date: February 24, 2017; Accepted date: March 16, 2017; Published date: March 20, 2017
Copyright: © 2017 Mans DRA, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.
Abstract
The parasitic disease leishmaniasis is caused by protozoa of the genus Leishmania which are transmitted by
sand fly vectors of the genus Phlebotomus in the Old World and Lutzomyia in the New World. Transmission can
either be anthroponotic (human to human) or zoonotic through mammalian reservoirs such as dogs and rodents.
Leishmaniasis has three principal clinical manifestations, namely cutaneous leishmaniasis (CL), mucocutaneous
leishmaniasis (MCL), and visceral leishmaniasis (VL). The cutaneous form characteristically causes skin ulcers, the
mucocutaneous form manifests as lesions of skin, mouth, and nose, and the (potentially lethal) visceral form affects
the internal organs such as spleen and liver and also invades the bone marrow. Leishmaniasis is endemic in about
ninety-eight countries and the diverse types of the disease occur in different regions of the world. CL is most
common in Afghanistan, Algeria, Pakistan, Iran, Brazil, and Colombia; MCL is mainly restricted to countries of the
Amazon Basin; and VL is most frequently seen in the Indian sub-continent, the Horn of Africa (Sudan and Ethiopia),
and Brazil. The current global prevalence is estimated at about 12 million, and each year, the disease in one of its
forms makes about 2 million new victims and claims up to 50,000 fatalities. This paper presents epidemiological,
biological, and clinical aspects of leishmaniasis throughout the world; then focuses on the disease in the Republic of
Suriname (South America); addresses in more detail the species of Leishmania parasites in that country; and
concludes with potential future directions to improve our understanding of leishmaniasis in Suriname.
Keywords: Leishmaniasis; Epidemiology; Biology; Clinical aspects;
Suriname;
Leishmania
species
Introduction
Leishmaniasis is a complex of parasitic diseases caused by
kinetoplastid agellates of the genus
Leishmania
(Trypanosomatidae)
[1,2] (Figure 1). ese obligate intracellular protozoa are transmitted
via infected female sand ies which are about one-third to half the size
of a mosquito (Figure 2). ere are a number of mammalian reservoir
hosts including man [3,4]. Based on their location in the sand y’s gut
during their development, two subgenera can be distinguished, namely
the subgenus
Leishmania
(
Leishmania
) which develops in the sand
y’s midgut, and the subgenus
Leishmania
(Vianna) which develops in
its hindgut [5]. Phylogenetic studies have conrmed this distinction
[6].
Leishmaniasis manifests as three principal clinical forms, namely
cutaneous leishmaniasis (CL), mucocutaneous leishmaniasis (MCL),
and visceral leishmaniasis (VL) [7]. ese are found in more than
ninety countries on every continent except Australia and Antarctica
[7]. CL and VL are the main forms of the disease in the Old World (the
Eastern Hemisphere), particularly in parts of Asia, the Middle East,
tropical Africa, North Africa, and southern Europe [7,8]. All three
forms are encountered in the New World (the Western Hemisphere),
mostly in parts of Mexico, Central America, and South America with
the exception of Chile and Uruguay [7,8].
Leishmania
parasites
ourish in ecological niches ranging from rain forests to deserts [7,8]
and are more common in rural areas and the outskirts of
municipalities than in metropolitan areas [7,8]. Most infections occur
during twilight, evening, and night-time hours, when the sand y
vectors are in general most active [7,8].
Figure 1: Taxonomic position of
Leishmania
spp. in the kingdom of
the protists.
Journal of Clinical & Experimental
Dermatology Research Mans et al., J Clin Exp Dermatol Res 2017, 8:2
DOI: 10.4172/2155-9554.1000388
Review article OMICS International
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
Figure 2: Female sand y specimen.
Infections in the Old and the New World are caused by distinct
Leishmania
species [8]. For instance, CL in the Old World is caused by,
among others,
L.
(
L
.)
tropica
and
L.
(
L
.)
major
, and in the New World
by, among others, the
L.
mexicana
species complex encompassing
L.
(
L
.)
mexicana
,
L.
(
L
.)
amazonensis
, and
L.
(
L
.)
venezuelensis
, as well as
the
L
.
braziliensis
species complex (also known as the subgenus
Viannia
) comprising
L
. (V.)
braziliensis
,
L.
(
V
.)
guyanensis
,
L.
(
V
.)
panamensis
, and
L.
(
V
.)
peruviana
[8]. MCL is - as mentioned above -
restricted to the New World where it is mainly caused by
L.
(
V
.)
braziliensis
[8]. VL is most frequently caused by the two members of
the
L
.
donovani
complex, namely
L.
(
L
.)
donovani
and
L.
(
L
.)
infantum
(known as
L.
(
L
.)
chagasi
in the New World) [8].
Leishmaniasis is the second leading cause of parasite-related deaths
aer malaria, causing 62,500 of the total number of 1,000,700 fatalities
attributable to parasitic diseases in 2013 [9]. An astonishing 350
million individuals are at risk of getting infected [10], particularly
those living under poor circumstances in tropical and subtropical
developing countries [11-13] and/or war-torn countries such as
Afghanistan [14], Sudan [15], Iraq [16], and more recently, Syria [17].
e current global prevalence exceeds 12 million, each year more than
2.5 million new cases are diagnosed [10], and the estimated disease
burden is 2.4 million disability-adjusted life years [10,18]. As a result,
the World Health Organization has classied leishmaniasis as a
category 1 disease - an emerging and/or uncontrolled disease -
acknowledging it as a severely neglected condition and emphasizing
the need of research programs to improve vector control, diagnostics,
and therapeutic arsenal to contain further morbidity and mortality
[10,18].
is paper gives some background on the biology, transmission,
pathology, diagnosis, treatment, and prevention and control of
leishmaniasis throughout the world; provides some relevant details
about this disease in the Republic of Suriname (South America);
addresses in more detail the species of
Leishmania
parasites as well as
their sand y vectors and mammalian reservoirs in that country with
respect to the rest of South America; and concludes with a few
suggestions for future lines of research.
Background
Biology
Leishmaniasis in humans can be caused by about twenty-one of the
thirty
Leishmania
parasite species known to infect mammals [1,2].
Among these are the species within the L. donovani complex; those
within the
L.
mexicana complex;
L
. (
L
.)
tropica
;
L
. (
L
.)
major
;
L
. (
L
)
aethiopica
; and the members of the
Viannia
subgenus [5,7]. All of them
have dierent degrees of virulence and cause distinct clinical courses
[5,7]. is makes the choice of treatment regimen dicult, because
dierent
Leishmania
(sub-) species respond dierently to selected
therapies [5,7]. Furthermore, certain forms of treatment are associated
with signicant toxicity [19], while the emergence of drug resistance is
an additional reason for concern [20,21].
e dierent
Leishmania
species are morphologically
indistinguishable, but can be dierentiated on the basis of
geographical, biological, molecular, and clinical features [5,7,8]. More
exact species identication requires very sensitive methods which are
based on isoenzyme analysis, molecular assays, and the use of
monoclonal antibodies [1,6]. However, all
Leishmania
species are
unicellular eukaryotes with a well-dened nucleus and other cell
organelles including a characteristic kinetoplast and agella (Figure 3)
[22,23]. e kinetoplast is a unique structure that is only found in
protozoa of the order Kinetoplastida [22,23]. It is formed by a mass of
DNA (circles or networks) inside the single large mitochondrion,
contains many copies of the mitochondrial genome and lies usually
adjacent to the agellar basal body (Figure 3; [22,23]).
Figure 3: Macrophage infected with
Leishmania
spp. clearly
showing nuclei and kinetoplasts.
As mentioned above,
Leishmania
species are digenetic or
heteroxenous parasites whose life cycle involves two hosts, a
(mammalian) vertebrate and an invertebrate (a sand y) [3,4].
Mammalian reservoirs for
Leishmania
parasites include wild animals
such as marsupials and opossums [24,25]; anteaters and sloths [26,27];
armadillos [28,29]; hyraxes [30]; various rodents including the spiny
rat [31], the water rat [32], the agouti [33], and the climbing mouse
[34]; some carnivores such as the crab-eating fox [35], the kinkajou
[36], and the hog-nosed skunk [37]; primates such as the red-crested
tamarin [38], the three-striped night monkey [39], and the red-faced
spider monkey [40]; as well as certain bats [41]. Importantly, because
of their close contacts with humans, domestic animals such as dogs
[42-45], cats [46,47], and horses [48,49] can also function as
mammalian reservoir for
Leishmania
spp.
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 2 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
Figure 4: Promastigote (top) and amastigote forms (bottom) of
Leishmania spp.
At least ninety-three sand y species are proven or probable vectors
of
Leishmania
parasites worldwide [7,8,35,50]. However, those that
transmit
Leishmania
parasites to humans comprise about thirty species
from the genus
Phlebotomus
in the Old World and
Lutzomyia
in the
New World [7,8,36,50]. Depending on the stage of their lifecycle, the
parasites exist as intracellular amastigotes in the vertebrate reservoir or
as extracellular promastigotes in the sand y (Figure 4; [51-53]). e
amastigote forms reside in macrophages and other types of
mononuclear phagocytic cells and the circulatory system of vertebrates
including humans [51-53]. ey are immobile, spherical to oval in
shape, measure 3 to 6 µm in length and 1 to 3 µm in width, and have a
short agellum that is embedded at the anterior end without projecting
out (Figure 4). e promastigote forms are found in the alimentary
tract of sand ies [5,51-53]. ey are motile, considerably larger than
the amastigote forms, and elongated, measuring 15 to 30 µm in length
and about 5 µm in width (Figure 4).
A long agellum (with a length of about the body length) projects
externally at the anterior end (Figure 4).
Figure 5: Leishmaniasis is transmitted by the bite of infected female
phlebotomine sandies. e sandies inject the infective stage (i.e.,
promastigotes) from their proboscis during blood meals (1).
Promastigotes that reach the puncture wound are phagocytized by
macrophages (2) and other types of mononuclear phagocytic cells.
Progmastigotes transform in these cells into the tissue stage of the
parasite (i.e., amastigotes (3) , which multiply by simple division
and proceed to infect other mononuclear phagocytic cells (4).
Parasite, host, and other factors aect whether the infection
becomes symptomatic and whether cutaneous or visceral
leishmaniasis results. Sandies become infected by ingesting
infected cells during blood meals (5,6). In sandies, amastigotes
transform into promastigotes, develop in the gut (7) (in the hindgut
for leishmanial organisms in the Viannia subgenus; in the midgut
for organisms in the Leishmania subgenus), and migrate to the
proboscis (8) (from https://www.cdc.gov/parasites/leishmaniasis/
biology.html).
Transmission cycle
When a female sand y takes a blood meal from an infected
mammalian, it takes up the amastigotes in the mononuclear
phagocytes from the prey’s circulation [51-53]. In the sand y’s midgut
(subgenus
Leishmania
) or hindgut (subgenus
Viannia
), the amastigotes
develop into promastigotes which attach to the gut wall and multiply
by longitudinal binary ssion [51-53]. Aer approximately one week
they transform into the infective metacyclic promastigotes which
migrate forward to the sand y’s foregut and proboscis [51-53].
When the sand y feeds again, it regurgitates the metacyclic
promastigotes into the bite site, introducing them into the circulation
of the new host [51-53]. ere, the promastigotes are phagocytized by
macrophages of the reticuloendothelial and lymphoid systems of skin,
nasopharynx, or viscera, depending on the parasite species [51-53].
e parasites survive within the phagosomes, resisting digestion by
lysosomal enzymes, transform into amastigotes, multiply and grow,
rupture the host cell, and release their progeny to infect new
macrophages including circulating monocytes, continuing the
infection cycle [51-53]. Clinical disease becomes apparent within
weeks to months aer infection, depending on the (sub-)species of
parasite and the host’s immune status [51-53]. Figure 5 gives a
schematic representation of the transmission cycle of leishmaniasis.
Pathology
As mentioned earlier,
Leishmania
infection can result in three main
clinical manifestations depending on species, geographic region, and
host immune response, namely CL, MCL, and VL [1,2,3,7,54,55].
ese disease forms result from infection of macrophages in the
dermis, the naso-oropharyngeal mucosa, and the reticuloendothelial
system, respectively [51-53]. All three forms can remain silent but can
cause severe morbidity, and, in the case of VL, even death [1,2,3,7].
Sometimes lesions heal spontaneously (particularly in the case of CL),
conferring immunity to the host against re-infection [54].
CL (Figure 6) is the most common manifestation of the disease -
particularly localized disease when compared to diuse and
disseminated CL-and is in general less severe than MCL and VL but
can cause considerable mutilation [54]. e disease occurs in eighty-
two countries throughout the world with the vast majority of cases
seen in Afghanistan, Algeria, Iran, Iraq, Syria, Saudi Arabia, Brazil,
Colombia, and Peru [56]. Most infections in the Old World are caused
by
L
. (
L
.)
tropica
,
L
. (
L
.)
major
, and
L
. (
L
.)
aethiopica
, as well as
L
. (
L
.)
infantum
and
L
. (
L
.)
donovani
[7,8] and in the New World by the
L.
mexicana
and the
L. braziliensis
species complex [7,8]. CL oen
manifests as localized disease which, however, may give rise to more
than one primary lesion, satellite lesions, regional lymphadenopathy,
and/or nodular lymphangitis [1,7,54]. Infected macrophages
containing amastigotes are found primarily at the site of infection
around the sores [1,7,54]. e lesions usually develop within weeks to
months aer the sand y bite, and may persist for months or even
years [1,7,54]. ey typically start as papules, progress to nodular
plaques, and end up as painful, volcano-shaped ulcerative lesions with
a raised border and central depression [1,7,54]. e healing process
commonly results in atrophic scarring [1,7,54].
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 3 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
Figure 6: Typical case of cutaneous leishmaniasis (from http://
www.dragony75.com/leish/leish.html).
MCL (Figure 7) is a less common clinical manifestation of
leishmaniasis compared to CL and VL [2,3]. It is a New-World disease
that is mostly encountered in Latin America, particularly Brazil,
Bolivia, and Peru [8]. It is mainly caused by species in the
L.
braziliensis
complex but can also be caused by
L
. (
L
.)
amazonensis
[1-3,5,7]. MCL occurs as a sequela of untreated or sub-optimally
treated CL, enabling parasites to spread from the skin, progressively
destroying the mucous membranes of the nasopharynx and
surrounding tissues leading to severe facial disgurement [1,7,54].
MCL has an incubation period of anywhere between one month and
twenty-four years [1,7,54]. e initial infection is a small red papule
that ulcerates in a few weeks, giving at and oen exuding lesions
[1,7,54].
Figure 7: Severe case of mucocutaneous leishmaniasis (from http://
www.parasiteswithoutborders.com/about/).
VL (Figure 8 is a slow but progressive illness and the most severe
form of leishmaniasis that is invariably fatal if le untreated [3,54,55].
is disease is prevalent in seventy countries throughout the world
with more than 90% of cases (about 300,000 per year) occurring in
India, Bangladesh, Nepal, Sudan, and Brazil [56]. e worldwide
mortality due to VL has been estimated at 20,000 to 40,000 [9]. VL is
usually caused by
L.
(
L
)
donovani
and
L
. (
L
)
infantum
and develops
following invasion of the parasites and congregation of infected
macrophages into the lymphatic tissues including bone marrow and
viscera (particularly liver and spleen), producing hepatosplenomegaly,
edema, and anemia [2,5,7,55]. Other characteristic symptoms are fever,
cachexia, pancytopenia, a high total protein level and a low albumin
level with hypergammaglobulinemia, as well as lymphadenopathy
[2,5,7,55]. VL oen develops within months of the sand y bite
[2,5,7,62], but asymptomatic infection can become clinically manifest
years to decades aer the exposure, particularly in
immunocompromised individuals [2,5,7,55].
Figure 8: Child with visceral leishmaniasis with
hepatosplenomegaly (from http://www.emedmd.com/content/
leishmaniasis)
Post kala-azar dermal leishmaniasis (PKDL) is a sequela of VL
characterized by macular, maculopapular, and nodular eruptions that
may develop mainly on the face, arms, and upper part of the trunk of
patients who apparently had successfully been treated for VL [57].
PKDL is mainly seen in Sudan [58] and India [59] in patients who had
recovered from infection by
L
. (
L
.)
donovani
, the principal causative
agent of VL in these countries [8]. In Sudan, it develops in about 50%
of these patients within 0 to 6 months aer their recovery but most
cases heal spontaneously [58]. In India, on the other hand, PKDL
occurs in 5 to 10% of former VL patients, manifests two to three years
aer their recuperation, and in general requires treatment [59]. In both
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 4 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
cases, the patients-even though completely cured from VL-may play a
role in the transmission of the disease [60].
Diagnosis
e diagnosis of leishmaniasis is based on clinical features
(supported by epidemiological data) and laboratory testing. Numerous
diagnostic methods have been described with a large variation in
diagnostic accuracy, including direct parasitological examination
(microscopy, histopathology, and parasite culture) and/or indirect
testing with serology and molecular diagnostics.
e laboratory diagnosis of CL (and MCL) is largely based on the
direct microscopic demonstration of
Leishmania
parasites or DNA in
skin scrapings or biopsy specimens (Figure 9; [61-63]). In the case of
suspected VL, usually a physical exam for signs of an enlarged spleen
or liver is rst performed which, if positive, is followed by microscopic
examination of a bone marrow biopsy or a blood sample for the
presence of
Leishmania
parasites or DNA [64,65]. Examination of a
bone marrow sample is more accurate than most serologic assays
which do not reliably distinguish between active and past infection
[64,65].
Figure 9: Light-microscopic examination of a stained bone marrow
specimen from a patient with VL showing a macrophage containing
multiple Leishmania amastigotes. e red arrow indicates the
amastigote’s nucleus, the black arrow its kinetoplast (from http://
www.cdc.gov/parasites/leishmaniasis/health_professionals/).
Parasite culture in tubes containing Novy-MacNeal-Nicolle medium
from clinical samples [66,67] is dicult, requires signicant technical
expertise, is prone to contamination, and is time-consuming. e
sensitivity of culture also tends to be low and highly variable [66,67].
A particular diagnostic approach for CL is the use of the
Leishmania
intradermal skin test (LST) or Montenegro skin test (MST), a marker
of cellular immune response [72]. e LST is occasionally used in CL
diagnosis (for instance, in epidemiological surveys and vaccine studies)
because of its relative simplicity and high sensitivity [73]. Its main
disadvantages are the requirement of culture facilities to produce the
MST antigen, the dierent impact of dierent antigen preparations on
test sensitivity, and the failure to distinguish between past and present
infections [74].
Current serological tests for leishmaniasis are mainly based on
formats such as indirect uorescent antibody (IFA; [71]), enzyme-
linked immunosorbent assay (ELISA; [72]), western blotting [73],
lateral ow assay [74], and direct agglutination test (DAT; [75]. ese
tests are not widely used for the diagnosis of CL, but particularly the
DAT is considered the serological standard for VL [76].
Many molecular diagnostic tests have been developed for the
diagnosis of leishmaniasis, as these have excellent sensitivity and
specicity and may allow for the use of less invasive sampling for
diagnosis [61-64]. In particular PCR has been widely exploited, either
as a single test [77], in a nested format [78], or as a quantitative assay
[79].
As there are no dened generally accepted protocols and almost
each laboratory applies its own in-house method, a head-to-head
comparison of the dierent PCR methods would be required for the
general implementation of this technology in routine diagnosis.
Furthermore, PCR requires adequate research infrastructure
(equipment, electricity) and technically skilled operators, making this
diagnostic platform less suitable for resource-restricted laboratories in
disease-endemic countries [61-64].
Application of isothermal diagnostic platforms that have been
developed in the last years could circumvent these requirements. For
example, nucleic acid sequence-based amplication (NASBA), an
isothermal reaction targeting parasite RNA, has been developed for
leishmaniasis [80]. Combined with oligo-chromatography (OC) for
post-amplication analysis further avoids the use of complex
equipment while preserving appropriate diagnostic performance
characteristics [81]. Furthermore, loop-mediated isothermal reaction
(LAMP) that is performed at 60 and 65 °C, has a very high specicity,
because it uses six primers and the end-product can be directly
visualized using simple detection methods [82].
Treatment
Some cutaneous infections do not require medication and lesions
heal spontaneously [54,83,84], but all cases of MCL and VL should be
treated [1,2,62,63,65,85]. However, there are no universal medical
protocols for managing the various clinical manifestations of
leishmaniasis [1,2,62,63,65,85]. Rather, treatment is oen
individualized, the choice depending on the infecting parasite species,
the status of the patient’s immune system, and the geographic location
the infection has been acquired [1,2,62,63,65,85]. Notably, even
therapeutic approaches found eective against a certain
Leishmania
species in a particular area do not always function in other situations
[1,2,62,63,65,85]. For example, data from clinical studies of therapy for
VL in a certain geographical area are not necessarily directly applicable
to VL caused by the same
Leishmania
species in other regions, to VL
caused by other
Leishmania
species, or to treatment of CL and MCL
[1,2,62,63,65,85].
e variation in clinical responses is probably partially attributable
to the dierences in the sensitivity of dierent
Leishmania
species to
available therapies [86]. e mechanisms involved in this phenomenon
are still unclear, largely because of our incomplete understanding of
the mechanisms that enable
Leishmania
parasites to evade or exploit
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 5 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
host immune defenses and to persist in host cells incomplete [87].
Contributing to the variation in clinical responses is the emergence of
drug resistance due to the use of inecacious drugs, sub-therapeutic
drug dosages and/or drug administration schedules, and/or poor
patient compliance [1,2,85,88]. Complicating the treatment of
leishmaniasis even more is the realization that special groups such as
young children, elderly persons, pregnant/lactating women, and
immunocompromised individuals and those suering from other
comorbidities may need adjusted or entirely dierent medications or
dosage regimens [1,2,85,88]. Unfortunately, however, many endemic
areas lack the nancial means to acquire a broad inventory of useful
drugs and develop an ecient healthcare infrastructure to eectively
manage all the dierent clinical variants of leishmaniasis [7,12].
e treatment approach of CL is mainly governed by the risk for
mucosal dissemination as well as the number, size, location, evolution,
and other clinical characteristics of the patient’s skin lesions
[1,2,62,85]. e options that are available include local therapy
involving heat and cryotherapy, as well as systemic parenteral and
systemic oral therapy. e drugs of rst-choice in most countries are
pentavalent antimonals such as sodium stibogluconate and meglumine
antimoniate. Frequently used alternatives are miltefosine and
pentamidine isethionate. As these drugs cause substantial toxicity and
side-eects [1,2,62,85] and the majority of cases of CL heal
spontaneously [72], the potential risks and benets of treatment must
be balanced by an experienced dermatologist for each CL patient
[1,2,62,85].
Local therapy involves cryotherapy using liquid nitrogen [89,90],
thermotherapy using localized current eld radiofrequency heat
[91,92], intralesional administration of pentavalent antimonials
[93,94], and/or topical application of a paromomycin ointment [95,96],
either alone or at certain combinations [62,85,89,90,97]. Local
treatment modalities are applicable in cases of CL of a few (less than
ve) lesions or without risk to develop into mucosal disease [86]. ese
cases comprise CL caused by Old World species such as
L
. (
L
.)
tropica
and
L
. (
L
.)
major
[91,92], CL caused by New World species that do not
cause MCL such as
L
. (
V
.)
nai
,
L
. (
L
.)
chagasi
, and
L
. (
L
.)
mexicana
[98,99], as well as uncomplicated cases of CL caused by
L
. (
V
.)
guyanensis
,
L
. (
L
.)
panamensis
, and
L.
(
L
.)
amazonensis
[86].
Systemic treatment of CL can be considered for disguring facial
lesions, lesions at sites that make topical treatment less desirable,
multiple lesions, and lesions caused by
Leishmania
species associated
with MCL [62,85,97]. For the latter reason, systemic pentavalent
antimonials are the gold standard treatment for New World CL which,
with the exception of CL caused by
L
. (
L
.)
mexicana
, carries the risk of
mucosal involvement [1-3,7]. us, these compounds are the drugs of
choice for treating CL caused by
L
. (
V
.)
braziliensis
, in addition to
MCL caused by
L
. (
L
.)
panamensis
,
L
. (
L
.)
amazonensis
, and
L
. (
V
.)
guyanensis
[86]. Alternative systemic treatments for New World CL
are oral miltefosine and parenteral amphotericin B, but these
compounds have important drawbacks. e clinical ecacy of
miltefosine shows geographic variations [100-102] and this compound
is, due to the existence of resistance, even not active against CL caused
by
L
. (
L
.)
mexicana
[103]. e latter compound causes considerably
more serious side-eects and is quite expensive [104]. In the Old
World, parenteral antimonials are considered second-line systemic
treatment for multiple or complicated CL lesions, caused by, for
instance,
L
. (
L
.)
major
[62,85,97]. Instead, such patients are given
(oral) miltefosine [105,106].
Systemic pentamidine isethionate is regulalrly used for treating CL
in South America [107,108]. is compound is also the treatment of
choice for the cutaneous lesions caused by
L. (V.) guyanensis
in French
Guiana and Suriname [35,109,110]. In Suriname, pentamidine
isethionate is in use since 1994 and is the only treatment option for CL
by
L
. (
V
.)
guyanensis
[109]. It is given as 3 intramuscular injections of
300 mg in 7 days [109] but is not eective in about 25% of CL patients
[109,111,112]. e possibility that the unsatisfactory responses were
attributable to infections by unreposive varaiants of
L
. (
V
.)
guyanensis
,
unresponsive
Leishmania
species other than
L
. (
V
.)
guyanensis
, and/or
poor therapy compliance needs to be veried.
VL is always treated systemically, along with adequate supportive
care involving, for instance, therapy for malnutrition, anemia and
bleeding, inter-current infections [1,2,85,88], and sometimes also HIV
co-infection [1,2,85,88]. As there is no eective vaccine available, the
clinical management of VL is solely based on chemotherapy using
mainly pentavalent antimonals; amphotericin B and its analogues,
particularly liposomal amphotericin B; oral miltefosine; and
paromomycin [1,2,85,88]. Similarly to their use against CL, most of
these drugs are not ideal for treatment of VL, causing serious side-
eects, evoke resistance, are very costly, require prolonged treatment,
and/or must be prepared and administered by complicated procedures
[1,2,85,88].
For many years, systemic therapy with the pentavalent antimonials
sodium stibogluconate and meglumine antimonate was-similarly to
that of CL-the treatment of choice for VL [1,2,85,88]. ese
compounds are given parenterally and cause serious side-eects
including high cardiotoxicity, joint and muscle pain, pancreatitis, and
nephrotoxicity [1,2,85,88]. Nevertheless, they have proven successful
for treating VL in endemic areas in Africa, South America, and Asia
[1,2,85,88]. e notable exception is VL caused by
L
. (
L
.)
donovani
in
parts of India and Nepal, where up to 65% of cases are highly resistant
to pentavalent antimonials [113,114]. is has been attributed to
inadequate dosing and treatment duration, poor patient compliance
[113,114] as well as the anthroponotic transmission of VL infection
which increases the chances for the rapid spread of resistant parasites
among humans [115]. Antimonials are still widely used for treating
VL, but require four weeks of hospitalization for daily IM injections
and monitoring the severe adverse events [1,2,85,88]. Of note, low
rates of antimonial resistance have also been reported in other
endemic areas such as Sudan [116].
Amphotericin B deoxycholate is a highly eective alternative for
pentavalent antimonials in the treatment of VL [117]. However, this
compound is highly toxic, causing among others, infusion reactions,
nephrotoxicity, hypokalemia, and myocarditis [118]. ese adverse
eects can be partially circumvented by careful and slow intravenous
administration [118]. Amphotericin B deoxycholate is also
recommended for the treatment of PKDL in the Indian subcontinent
[118].
Lipid amphotericin B formulations for treating VL with improved
bioavailability and pharmacokinetic properties and less toxicity when
compared to amphotericin B deoxycholate [119-121] are liposomal
amphotericin B, amphotericin B lipid complex, and amphotericin B
colloidal dispersion. However, these compounds displayed
considerable geographical variation in their total dose requirements for
clinical ecacy: from 10 mg/kg in India [122] to 18-21 mg/kg in the
Mediterranean and South America [123-125] and 30 mg/kg in East
Africa [126]. Nevertheless, liposomal amphotericin B has become an
approved treatment for VL with less toxicity, a better half-life, and a
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 6 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
high level of ecacy (a 90% cure rate) when compared to the parent
compound [119,120]. In the Mediterranean basin, for instance, it is the
treatment of choice for immunocompetent VL patients [127]. Its main
limitations are its high cost, the necessity of slow IV administration,
and its lack of stability at high temperature (cold chain is needed).
Miltefosine was the rst eective oral treatment for VL [128],
showing ecacy in both antimony-responding and -non-responding
patients [129]. Oral miltefosine is the rst choice for treating VL in
various endemic regions in Africa and Asia [128], has been
recommended as rst-line drug for childhood VL [130], and is also
ecacious against PKDL [131,132]. e most notable side-eects of
this compound are gastrointestinal manifestations, hepatotoxicity, and
nephrotoxicity which are, fortunately, manageable [133]. However, its
potential teratogenicity is an important problem, while its very high
price prohibits its widespread use in the populations most in need
[133]. e combination of miltefosine with amphotericin B or with
paromomycin may be helpful against antimony-resistant VL infections
[134].
Paromomycin sulphate was approved in India for the treatment of
VL in August 2006 [135]. Subsequent clinical trials in Kenya, Sudan
and India showed that this drug, either singly or in combination with
sodium stibogluconate was highly ecacious against VL [136-139]. Its
manageable side-eects (mainly pain at the injection site, reversible
ototoxicity, and reversibly raised hepatic transaminases) and its
relatively low cost (about US $10 per case) represent important
advantages [140,141]. However, its parenteral administration make its
broad use in control programs of a developing country unfeasible
[140,141], while its use as a single agent may lead to the development
of resistance [140,141]. Despite limited experience with paromomycin
sulphate for VL in the Mediterranean and Latin America-where
L. (L.)
infantum
is the causative agent [7,8] - it is an accepted alternative
against VL that is resistant to the above-mentioned antileishmanial
drugs [88,142].
Pentamidine isethionate was originally used as second-line drug in
India to treat refractory VL [1,2,87,90] but was discontinued because
of declining ecacy due to the emergence of resistance [114,143] as
well as the occurrence of serious toxicities such as insulin-dependent
diabetes mellitus [144]. However, PI is still used in combined therapies
for VL [145].
Prevention and control
In various urban endemic areas where the transmission cycle is
zoonotically maintained by dogs, reducing the size of these reservoirs
has been attempted as a means to contain further spread of the disease
[146]. However, this approach has not always proven eective and may
be considered unethical [147]. In forested areas away from human
habitation, the reservoir hosts are wild animals, and prevention of sand
y bites is even more dicult. Preventive measures may include
protection from sand y bites, for instance, by avoiding nocturnal
outdoor activities as much as possible, wearing protective clothing, and
applying insect repellent to exposed skin, and insecticidal sprays in
residences [148,149]. e use of bed nets impregnated with long-
lasting insecticides may also be helpful [150]. In areas with
anthroponotic transmission, early detection and eective treatment of
individual patients can help control the spread of the parasite [150].
Importantly, suboptimal treatment must be avoided at all costs, as this
can lead to the development and spread of drug resistance [150].
Spraying houses with insecticides and using impregnated bed nets is
also recommended [148,150].
Leishmaniasis in Suriname
Brief background on Suriname
e Republic of Suriname is located on the north-east coast of
South America and borders the Atlantic Ocean to the north, French
Guiana to the east, Brazil to the south, and Guyana to the west (Figure
10). Despite its location in South America, Suriname is culturally
considered a Caribbean rather than a Latin American country and is a
member of the Caribbean Community (CARICOM) [151]. e climate
is tropical with abundant rainfall, a uniform temperature of on average
27°C, and a high relative humidity of 81% in the capital city of
Paramaribo [152]. ere are four seasons, namely the long rainy
season (April through July), the long dry season (August through
November), the short rainy season (December through January), and
the short dry season (February through March) [152].
Figure 10: Map of the Republic of Suriname. Insert shows
localization of Suriname in South America (from http://
www.istanbul-visit.com/carte/suriname-carte.asp).
Suriname’s surface area of roughly 165,000 km2 can be distinguished
into a northern urban-coastal and rural-coastal area as well as a
southern-rural interior (Figure 10) [153]. Approximately 80% of the
population of almost 570,000 lives in Paramaribo and other cities in
the relatively narrow urban-coastal part of the country [153]. e
remaining 20% of Suriname’s inhabitants populates the rural-coastal
and southern-rural areas [153]. e latter region is referred to as the
hinterland, encompasses more than three-quarters of the country’s
land surface, and consists largely of sparsely inhabited savanna and
dense, pristine, and highly biodiverse tropical rain forest [153]. It is
furthermore, together with segments of Bolivia, Brazil, Colombia,
Ecuador, Guyana, Peru, and Venezuela, part of the Amazon Basin, the
area of South America that is drained by the Amazon River and its
tributaries and that encompasses about 7,500,000 km2 (i.e., roughly
40%) of that continent [154]. As a result, Suriname is one of the most
forested countries in the world [154,155].
e urban-coastal region is characterized by a ‘western’ lifestyle,
modern health-care facilities, and an economy that is mainly based on
commerce, services, and industry [156]. e rural-coastal and
southern-rural societies have a more traditional way of living, lack
comprehensive public health services, and have agriculture, forestry,
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 7 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
crude oil drilling, bauxite and gold mining, as well as ecotourism as
major economic activities [156]. ese activities have been growing in
scale and economic importance in recent years and are, together with
agriculture and sheries, the country’s most important means of
support, contributing substantially to the gross domestic income of U$
5.297 billion and the average per-capita income of U$ 9,583 in 2014
[156,157]. is positions Suriname among the upper-middle income
economies of the World Bank’s ranking [156,157].
Suriname uses around 6% of its gross domestic product for health
expenditures [159] which corresponds to U$ 589 per capita in 2014
[158]. e Minister of Health and the Director of Health (the Chief
Medical Ocer) are responsible for all aspects regarding health care in
the country [158]. Important subdivisions of the ministry are the
Bureau of Public Health which is in charge of, among others,
eradicating parasitic and microbial diseases; the Regional Health
Service and the Medical Mission which are responsible for primary
health care in the coastal area and the hinterland, respectively; and the
Dermatology Clinic that provides services for sexually transmitted
diseases, HIV/AIDS, and skin conditions including leishmaniasis
[158]. Secondary and specialist care are provided by two private and
two government-supported public hospitals in Paramaribo and one
public hospital in the western rural-coastal district of Nickerie [158].
Occurrence of leishmaniasis in Suriname
CL is the most common form of leishmaniasis in Suriname [159]
where it is generally known as ‘bosyaws’ or ‘busi yasi’ (meaning ‘disease
from the jungle’) [160]. e rst cases of CL in the country were
reported in 1911 [160]. Since then, CL has become an increasing
public health problem in Suriname and is generally considered an
endemic disease [109,159,161]. e incidence has been estimated at
5.45 per 1,000 for the hinterland and 0.68 per 1,000 for the entire
country [159] but no reliable epidemiological data are available. is is
due, among others, to the lack of information about risk groups such as
infected Brazilian gold miners who work (illegally) in the hinterland,
and infected Amerindians and Maroons in the hinterland who treat
themselves [162,163].
CL in Suriname is maintained by a zoonotic cycle in which the sand
y vectors exist in close association with the
Leishmania
parasites and
a variety of wild mammalians believed to serve as reservoir hosts
including the two-toed sloth, the anteater, and several species of
marsupials and rodents [35]. Although domestic animals such as cats,
horses, and dogs may also assume the role as reservoir host [43,46],
most infections occur in the forested hinterland when the victims (like
tribal people, personnel form gold mining, bauxite mining, and
logging companies; eco-tourists; as well as recreational shers and
hunters) intrude into the vectors’ habitats [159].
For many years,
L.
(V.) guyanensis was believed to be the only
Leishmania
species that caused CL in Suriname [159,161]. However, in
the past decades, a number of patients presented with clinical forms of
the disease that behaved dierently from that associated with this
parasite species. e presumption that there were other
Leishmania
species present in Suriname was conrmed by PCR-based methods
identifying a few cases of leishmaniasis caused by
L
. (
V
.)
lainsoni
[159],
L.
(
V
.)
nai
[164],
L
. (
V
.)
braziliensis
[165], and
L.
(
L
.)
amazonensis
[159,166]. At the same time, sand y species associated
with the transmission of CL by all the above-mentioned
Leishmania
species were detected in high-transmission areas of CL in Suriname
[167,168]. Hereunder, the various
Leishmania
species identied in
Suriname are addressed in more detail.
Leishmania
species in Suriname
L. (V.) guyanensis
L. (V.) guyanensisis
is most probably the principal
Leishmania
species in Suriname [109,159,160], being responsible for more than
90% of CL cases in the country and claiming roughly 200 victims per
year [159,165,166].
L. (V.) guyanensis
is also highly prevalent in French
Guiana and Northern Brazil and is, furthermore, found in various
other South America countries such as Guyana, Peru, Colombia, and
Ecuador [35,169-175]. In all these regions-but particularly in
Suriname, French Guiana, and Northern Brazil-infection by this
parasite is an important cause of CL [35,169-175]. In Columbia and
French Guiana, for instance, L. (V.) guyanensisis has been held
responsible for more than 95% of cases of CL [35,174]. And in areas
south of the Amazon River in Brazil it has also been associated with
MCL [176].
Several sand y vectors have been implicated in the spread of CL (or
MCL) by L. (V.) guyanensis in Suriname, including
Lu. umbratilis
,
Lu.
anduzei
,
Lu. migonei
, and
Lu whitmani
[168].
Lu. umbratilis
and
Lu.
anduzei
are proven vectors of the parasite in other parts of the Amazon
Basin such as French Guiana [35] and several areas in Brazil [177].
Lu.
anduzei
is, in addition, a suspected vector of
L. (V.) guyanensis
in
French Guiana, Guyana, Suriname, and Venezuela [178].
Lu. migonei
has been reported as a putative vector of
L. (V.) guyanensis
in
Venezuela [178]. And
Lu. whitmani
may function as a vector of this
Leishmania
species in the state of Amapá, Brazil [179].
Lu.
ayacuchensis
has been found in Peru naturally infected by
L. (V.)
guyanensis
promastigotes [175] but has not been encountered in
Suriname.
So far, only a few studies on reservoir mammalian species of
L. (V.)
guyanensis
have been conducted in Suriname. In one of these studies,
indications have been obtained to implicate the dog in the
transmission of CL-causing
Leishmania
species in Suriname [44].
However, these data were not conclusive [44], even though evidence is
accumulating that dogs and other domestic animals may serve as
reservoirs of CL caused by
L. (V.) guyanensis
in other parts of the
Americas [180,181]. Wild mammals believed to be important hosts of
L. (V.) guyanenesis
[29,35] such as sloths - including the two-toed sloth
Choloepus didactylus
- are present in Suriname, but also have not
conclusively been identied as reservoirs of the parasite in the country.
Remarkably, certain New World tree sloths are parasitized by another
vector of
Lu. umbratilis
, the intra-erythrocytic agellate
Endotrypanum
, which may complicate the diagnosis of leishmaniasis
[182].
Pentamidine isethionate is since 1994 the rst-line drug and the
only treatment option for CL caused by
L. (V.) guyanensis
in Suriname
[109,165]. It is given as three intramuscular injections of 300 mg on
days 1, 4, and 7 [109,165]. e infection responds in general favorably
to pentamidine isethionate [109,110] if not resolving spontaneously
[54,83,84], but, as mentioned above, accomplishes cures in only about
75% of patients [112,165]. is suggests that some of the infections
may be caused by
Leishmania
species other than L. (V.) guyanensis
which do not respond to pentamidine isethionate [159,164-166]. It is
also possible that the infections are caused by distinct populations of
L.
(V.) guyanensis
which behave dierently from each other with respect
to severity and dissemination of cutaneous lesions as well as response
to pentamidine isethionate. is has been reported for Suriname’s
neighboring country French Guiana, where CL may be caused by two
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 8 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
dissimilar populations of
L. (V.) guyanensis
which have a dierent
disease course and require dierent forms of treatment [183].
It is also possible that the unfavorable responses to pentamidine
isethionate are attributable to poor therapy compliance [184] or the
emergence of drug resistance [185,186]. Obviously, these factors may
lead to incomplete healing and therapy failure [184-186]. Clearly, these
issues must further be investigated. Meanwhile, in order to improve
response rates and compliance, a comparative clinical trial has assessed
the standard regimen of pentamidine isethionate IM 300 mg on days
1,4, and 7 with respect to a shorter but more dose-intensive regimen of
7 mg/kg on days 1 and 3 [165]. e results from this study showed that
the former regimen was not non-inferior to the latter, but less toxic
when compared to the latter [165]. For this reason, the 3 day-regimen
is still the mainstay in Suriname for treating CL caused by
L. (V.)
guyanenesis
.
L. (V.) lainsoni
CL in Suriname caused by infection with
L. (V.) lainsoni
was rst
reported in 2006 [159]. Using PCR-RFLP analysis of skin biopsies from
thirty-three patients with microscopically and/or PCR-conrmed CL,
one patient appeared infected by this parasite [159]. is
Leishmania
species is probably endemic in Suriname, as the infected patient had
never traveled outside the country [159]. Nevertheless, to our
knowledge, no other cases of CL caused by
L. (V.) lainsoni
have been
reported in Suriname, suggesting that this species has relatively little
clinical relevance.
Still,
L. (V.) lainsoni
is probably widely distributed in South
America. Aer its original identication in samples from infected
humans in the state of Pará in the Brazilian Amazon region [187],
L.
(V.) lainsoni
was detected in CL patients from other parts of Brazil
[188], the sub Andean regions of Peru [189] and Bolivia [190,191],
French Guiana [35], and the Ecuadorian Amazon [192] besides
Suriname [159].
Consistent with the identication of
L. (V.) lainsoni
in Suriname is
the identication of
Lu. ubiquitalis
in the country [168], a proven sand
y vector of
L. (V.) lainsoni
in Pará state, Brazil [33,193-195]. In
Yungas, Bolivia,
Lu. nuneztovari
anglesi
has been implicated in the
transmission of this parasite [191,196], but it has so far not been
encountered in Suriname. In the Brazilian Amazon region, the rodent
Agouti paca has been implicated as a reservoir host of
L. (V.) lainsoni
[33]. Although this mammalian is also present in Suriname its
involvement in the transmission cycle of CL by
L. (V.) lainsoni
in this
country Suriname remains to be veried.
L. (V.) nai
e rst cases of CL caused by
L. (V.) nai
in Suriname - three
Dutch male military who had been infected during jungle training in
the country - were reported in 2010 [164]. e infecting
Leishmania
species was identied in patient biopsies by microscopy of Giemsa-
stained smears, culture, and mini-exon repeat PCR [164]. e
identication in Suriname of a conrmed reservoir host (the nine-
banded armadillo
Dasypus novemcinctus
) as well as sand y vectors
implicated in the transmission of
L. (V.) nai
(
Lu. paraensis
[25,200],
Lu. ayrozai
[168], and
Lu. squamiventris
[168]), provided support for
L. (V.) nai
as a cause of CL in the country.
Of note,
Lu. ayrozai
is a proven vector of
L. (V.) nai
in Brazil
[35,201], and
Lu. squamiventris
is generally considered a vector of L.
(V.)
nai
in both French Guiana [35] and Brazil [29]. Furthermore,
L.
(V.) nai
, rst described as a parasite of
D. novemcinctus
in the
northern Brazilian state of Pará [28], was later conrmed to represent a
reservoir of this
Leishmania
species [25,29]. ese and other studies
also implicated the above-mentioned sand y species in the
transmission of CL in the Brazilian Amazon [25,29,202-204], French
Guiana [35], and the central Amazonian area Arajuno in Ecuador
[205].
In addition to Suriname,
L. (V.) nai
was identied as a cause of CL
in particularly Amazonian Brazil [25,29,188,203,206] as well as various
other Latin American and Caribbean countries [25,35,99,188,205-208].
ese observations suggest that
L. (V.) nai
is widespread in South
America [99], which is consistent with the presence of both hosts and
vectors in a wide geographical area in this continent [25]. Nevertheless,
as reported for other endemic parts of South America and the
Caribbean [25,29,35,188,203,205-208],
L. (V.) nai
also seems an
uncommon cause of CL in Suriname when compared to CL caused by
other
Leishmania
species [164].
L. (V.) braziliensis
e rst case-and so far the only one-of CL in Suriname due to
infection with
L. (V.) braziliensis
dates from 2012 [165]. e patient
was a 26 year-old male who had probably contracted the disease three
years before while on a hunting trip in Suriname’s hinterland [165]. A
PCR restriction fragment length polymorphism assay and nucleotide
sequencing conrmed that
L. (V.) braziliensis
was the causative agent
[165]. However, the infection showed no signs of mucosal involvement
and responded favorably to treatment with pentamidine isethionate
[165].
Infections by
L. (V.) braziliensis
are also encountered in other South
American countries in and around the Amazon Basin as well as most
of Central America [209,210]. In Ecuador, for instance,
L. (V.)
braziliensis
is probably the dominant CL-causing species besides
L. (V.)
guyanensis
, and the number of infections by this
Leishmania
species is
increasing in the Pacic coast areas of this country [171]. And
although
L. (V.) guyanensis
is, similarly to Suriname, the main cause of
CL in French Guiana, cases due to
L. (V.) braziliensis
are occasionally
encountered [35]. Importantly, in many countries in the New World,
L.
(V.) braziliensis
infections not only manifest as CL but also as MCL
[211,212], causing more cases of MCL than any other
Leishmania
species in these parts of the globe [214]. In the Amazon region, for
instance,
L. (V.) braziliensis
is the predominant cause of MCL
[169,210].
Several sand y vectors associated with the transmission of CL or
MCL by
L. (V.) braziliensis
have been detected in Suriname [168].
ese include
Lu. ayrozai
, a proven vector of
L. (V.) braziliensis
in
Bolivia [177];
Lu. whitmani
, a putative vector of
L. (V.) braziliensis
in
various parts of Brazil [214-216];
Lu. davisi
, found infected by
Leishmania
spp. in regions in Brazil considered endemic for
L. (V.)
braziliensis
[25,204];
Lu. migonei
, incriminated in the transmission of
CL by
L. (V.) braziliensis
in endemic areas in Brazil and Venezuela
[201,217-219]; and
Lu. intermedia
, considered the principal vector of
L. (V.) braziliensis
inside houses and in peridomiciliary premises in
Southeast Brazil [220-222].
e armadillo
Euphractus sexcinctus
and
A. paca
are presumed
mammalian reservoir hosts in the sylvatic cycle of
L. (V.) braziliensis
in
Espírito Santo, Brazil [223]. Dogs and possibly horses are believed to
be the most important vertebrate hosts in the peridomestic cycle of this
parasite [42]. e latter ndings may support the possible involvement
of the dog in the transmission of CL in Suriname [44]. However, in an
earlier study on the sand y fauna in high-transmission areas of CL in
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 9 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
Suriname [168], only one of the 2,743 captured sand y specimens
(belonging to 34 dierent species)-a female specimen of
Lu.
squamiventris (s.l.)
- was naturally infected with
L. (V.) braziliensis
.
Future studies should determine whether this sand y specimen was an
incidental or a secondary vector of the parasite.
L. (L.) amazonensis
L. (L.) amazonensis
was rst detected as a cause of CL in Suriname
in 2006, together with
L. (V.) lainsoni
[159]. To the best of our
knowledge, this is the only case in Suriname of CL caused by this
Leishmania
species. Nevertheless,
L. (L.) amazonensis
is probably,
together with
L. (V.) braziliensis
, among the most common
Leishmania
species in the Amazon region [169,211,224-227], being responsible for
about 8% of cases of human CL in Brazil [224].
L. (L.) amazonensis
has
also been encountered in various sub-Andean regions of Bolivia
[228-229].
Sand y species implicated in the transmission of
L. (L.)
amazonensis
are
Lu. aviscutellata
,
Lu. withmani
,
Lu. nuneztovari
anglesi
, and
Lu. migonei
.
Lu. aviscutellata
is a proven vector of
L. (L.)
amazonensis
in the Amazon basin [35] as well as other parts of Brazil
and South America [201,230,231]. Importantly, specimens of this sand
y species which were experimentally infected by
L. (L.) amazonensis
amastigotes produced infections in hamster skin [232].
Lu. withmani
and
Lu. nuneztovari
anglesi are suspected vectors of this parasite in the
state of Mato Grosso do Sul, Brazil [231], and Bolivia [233,234],
respectively. And
L. (V.) amazonensis
amastigotes developed normally
to promastigotes in experimentally infected
Lu. migonei
sand ies,
aer which the latter were able to transmit the infection to vertebrates
[235]. Up to now, there are no indications for any of these vectors
transmitting
L. (V.) amazonensis
in Suriname.
Mammalian reservoirs of
L. (L.) amazonensis
are probably small
rodents, marsupials, primates, and carnivores [226] including rice rats
and grass mice in Bolivia [228,233,234], and in Brazil, domestic dogs
[236]. e latter assumption is based on a case of canine leishmaniasis
caused by
L. (V.) amazonensis
in the Brazilian state of Paraná which is
considered endemic for CL in humans [2].
e identication of all four above-mentioned sand y species in
Suriname [168] and the possible involvement of the dog as a host
reservoir in the country [44], raise the possibility that
L. (L.)
amazonensis
may also be more abundantly present in Suriname.
Surinamese health authorities should be aware of this possibility,
because this parasite has not only been associated with spontaneously
healing cutaneous and diuse cutaneous CL [234], but also with
disseminated disease [234] and MCL [2,3,7,8]. In the State of Bahia,
Brazil, for instance, infection with
L. (L.) amazonensis
was associated
with various dierent clinical presentations including CL (20/49 cases),
MCL (5/13 cases), and VL (11/46 cases), as well as four cases of PKDL
[242].
Future directions
CL is the main manifestation of leishmaniasis in Suriname
[109,112,159,165] and
L. (V.) guyanensis
is most likely the principal
species causing this disease in the country [109,159,160]. However, a
few cases of CL caused by
L. (V.) braziliensis
and
L. (L.) amazonensis
have emerged in Suriname [159,165,166]. As both parasite species have
also been associated with more serious forms of leishmaniasis
[35,176,211-213,235], it is necessary to develop and implement proper
measures for diagnosing and treating cases of MCL that may emerge in
the country.
L. (V.) lainsoni
and
L. (V.) nai
have also been identied as
additional causes of CL in Suriname [159,164]. Even though there were
also only a few cases up to now [159,164], the wide presence of these
parasite species in South America [29,35,172, 187-194,203,205-208]
raises the possibility that they may contribute more to the burden of
CL in Suriname than one might think at rst sight. Indeed, infections
by these
Leishmania
species may remain undetected - similarly to
those caused by L. (V.) guyanensis [87,90] - because they respond to
parenteral antimony drugs and pentamidine isethionate or heal
spontaneously [1,2,87,159,164,203,207]. For these reasons, a series of
comprehensive studies should be initiated to identify the full spectrum
of
Leishmania
species present in Suriname and to determine their
impact on CL in the country.
Although previously suggested [44], it is not certain whether the
dog plays a role as a reservoir host in the transmission of CL in
Suriname. It is also not certain whether and which other domestic
animals [42-49] and wild animals [24-41] play a role in this
phenomenon in Suriname. Clearly, such eorts will both improve our
understanding of leishmaniasis in Suriname and contribute to
programs to combat this disease in the country. For the same reasons,
eorts following up the rst and so far the only comprehensive study
on the sand y fauna in high-transmission areas of CL in Suriname
[168] should be dedicated to identify the sand ies operating as vectors
of CL in Suriname.
ese surveys are all the more important when considering the
expanding geographical distribution of CL in Suriname as a result of
the growing economic activities and increasing deforestation in the
sand ies’ habitats in the country’s hinterland [156,157]. Given the
absence of ecacious drugs other than pentamidine isethionate in
[109,165], and the limited nancial resources of Suriname [156,157],
elimination of the disease poses a huge challenge for the country.
erefore, priority should be given to establishing eective control
programs based on extensive comprehension of the biology of CL.
Hopefully, these will help in the design of strategies to eectively target
the breeding and resting sites of the sand y vectors and successfully
control domestic and sylvatic mammalian reservoirs near human
dwellings.
References
1. Georgiadou SP, Makaritsis KP, Dalekos GN1 (2015) Leishmaniasis
revisited: Current aspects on epidemiology, diagnosis and treatment. J
Transl Int Med 3: 43-50.
2. Savoia D (2015) Recent updates and perspectives on leishmaniasis. J
Infect Dev Ctries 9: 588-596.
3. Desjeux P (2004) Leishmaniasis: current situation and new perspectives.
Comp Immunol Microbiol Infect Dis 27: 305-318.
4. Roque AL, Jansen AM (2014) Wild and synanthropic reservoirs of
Leishmania species in the Americas. Int J Parasitol Parasites Wildl 3:
251-262.
5. Lainson R, Shaw JJ (1987) Evolution, classication and geographical
distribution. In W Peters, E Killick-Kendrick (eds), e leishmaniases in
biology and medicine. Academic Press, London, p. 1-120.
6. Boite MC, Mauricio IL, Miles MA, Cupolillo E (2012) New insights on
taxonomy, phylogeny and population genetics of Leishmania (Viannia)
parasites based on multilocus sequence analysis. PLoS Negl Trop Dis 6:
e1888. DOI:10.1371/journal.pntd.0001888.
7. Dawit G, Girma Z, Simenew K (2013) A review on biology, epidemiology
and public health signicance of leishmaniasis. J Bacteriol Parasitol 4:166.
DOI:10.4172/2155-9597.1000166.
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 10 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
8. Kevric I, Cappel MA, Keeling JH (2015) New World and Old World
Leishmania Infections: A Practical Review. Dermatol Clin 33: 579-593.
9. GBD 2013 Mortality and Causes of Death Collaborators (2015) Global,
regional, and national age–sex specic all-cause and cause-specic
mortality for 240 causes of death, 1990–2013: a systematic analysis for the
Global Burden of Disease Study 2013. Lancet 385: 117-171
10. World Health Organization (2016) Leishmaniasis fact sheet (updated
September 2016). Retrieved February 2, 2017.
11. Ashford RW (2000) e leishmaniases as emerging and reemerging
zoonoses. Int J Parasitol 30: 1269-1281.
12. Alvar J, Yactayo S, Bern C (2006) Leishmaniasis and poverty. Trends
Parasitol 22: 552-557.
13. Hotez PJ, Molyneux DH, Fenwick A, Ottesen E, Ehrlich-Sachs S, Sachs JD
(2006) Incorporating a rapid-impact package for neglected tropical
diseases with programs for HIV/AIDS, tuberculosis, and malaria. PLoS
Medicine 3: e102.
14. Reithinger R, Mohsen M, Aadil K, Sidiqi M, Erasmus P, et al. (2003)
Anthroponotic cutaneous leishmaniasis, Kabul, Afghanistan. Emerg
Infect Dis 9: 727-729.
15. Seaman J, Mercer AJ, Sondorp HE, Herwaldt BL (1996) Epidemic visceral
leishmaniasis in southern Sudan: treatment of severely debilitated
patients under wartime conditions and with limited resources. Ann
Intern Med 124: 664-672.
16. Korzeniewski K, Pieniuta S (2011) Reasons for medical evacuation of
soldiers serving in Iraqi Freedom Operation. Int Marit Health 62: 77-81.
17. Du R, Hotez PJ, Al-Salem WS, Acosta-Serrano A (2016) Old World
cutaneous leishmaniasis and refugee crises in the Middle East and North
Africa. PLoS Negl Trop Dis 10 :e0004545.
18. Murray HW1, Berman JD, Davies CR, Saravia NG (2005) Advances in
leishmaniasis. Lancet 366: 1561-1577.
19. Davis AJ, Kedzierski L (2005) Recent advances in antileishmanial drug
development. Curr Opin Investig Drugs 6: 163-169.
20. Cro SL, Yardley V, Kendrick H (2002) Drug sensitivity of Leishmania
species: some unresolved problems. Trans R Soc Trop Med Hyg 96 Suppl
1: S127-129.
21. Cro SL, Sundar S, Fairlamb AH (2006) Drug resistance in leishmaniasis.
Clin Microbiol Rev 19: 111-126.
22. Shapiro TA, Englund PT (1995) e structure and replication of
kinetoplast DNA. Annu Rev Microbiol 49: 117-143.
23. Shlomai J1 (2004) e structure and replication of kinetoplast DNA. Curr
Mol Med 4: 623-647.
24. Lainson R, Shaw JJ, Povoa M (1981). e importance of edentates (sloths
and anteaters) as primary reservoirs of Leishmania braziliensis
guyanensis, causative agent of “pianbois” in north Brazil. Trans R Soc
Trop Med Hyg 75: 611-612.
25. Grimaldi G Jr, Momen H, Nai RD, Mahon-Pratt D, Barrett TV (1991)
Characterization and classication of leishmanial parasites from humans,
wild mammals, and sand ies in the Amazon region of Brazil. Am J Trop
Med Hyg 44: 645-661.
26. Lainson R, Braga RR, de Souza AA, Povoa MM, Ishikawa EA, Silveira FT
(1989) Leishmania (Viannia) shawi sp. n., a parasite of monkeys, sloths
and procyonids in Amazonian Brazil. Ann Parasitol Hum Comp 64:
200-207.
27. Grimaldi G Jr, Kreutzer RD, Hashiguchi Y, Gomez EA, Mimory T, Tesh
RB (1992) Description of Leishmania equatorensis sp. n (Kinetoplastida:
trypanosomatidae), a new parasite infecting arboreal mammals in
Ecuador. Mem Inst Oswaldo Cruz 87: 221-228.
28. Lainson R, Shaw JJ, Ward RD, Ready PD, Nai RD (1979) Leishmaniasis
in Brazil: XIII. Isolation of Leishmania from armadillos (Dasypus
novemcinctus), and obser vations on the epidemiology of cutaneous
leishmaniasis in north Para State. Trans R Soc Trop Med Hyg 73: 239-242.
29. Nai RD, Freitas RA, Nai MF, Arias JR, Barrett TV, Momen H, Grimaldi
Jr G. (1991) Epidemiological and nosological aspects of Leishmania nai
Lainson & Shaw, 1989. Mem Inst Oswaldo Cruz 86: 317-321.
30. Svobodova M, Votypka J, Kravchenko V, Ashford RW, Warburg A (2005)
e hyrax (Procavia capensis) is reservoir host of Leishmania tropica in
northern Israel. J Eukaryot Microbiol 52: 35S–38S.
31. Dedet JP1, Gay F, Chatenay G (1989) Isolation of Leishmania species
from wild mammals in French Guiana. Trans R Soc Trop Med Hyg 83:
613-615.
32. Peterson NE, Vexemat JA, Rosa ACOC, Lago PRL (1988) Isolation of
Leishmania (Viannia) braziliensis from the rodent Nectomys squamipes
captured in Bahia, Brazil. Mem Inst Oswaldo Cruz 83 : BI 28.
33. Silveira FT, Lainson R, Shaw JJ, Braga RR, Ishikawa EE, et al. (1991)
[Cutaneous leishmaniasis in Amazonia: isolation of Leishmania (Viannia)
lainsoni from the rodent Agouti paca (Rodentia: Dasyproctidae), in the
state of Pará, Brazil]. Rev Inst Med Trop Sao Paulo 33: 18-22.
34. Quaresma PF, Rego FD, Botelho HA, da Silva SR, Moura Junior AJ,
Teixeira Neto RG, Madeira FM, Carvalho MB, Paglia AP, Melo MN,
Gontijo CM (2011) Wild, synanthropic and domestic hosts of Leishmania
in an endemic area of cutaneous leishmaniasis in Minas Gerais State,
Brazil. Trans R Soc Trop Med Hyg 105: 579-585.
35. Rotureau B (2006) Ecology of the leishmania species in the Guianan
ecoregion complex. Am J Trop Med Hyg 74: 81-96.
36. Pajot FX, Le Pont F, Gentile B, Besnard R (1982) Epidemiology of
leishmaniasis in French Guiana. Trans R Soc Trop Med Hyg 76: 112-113.
37. Buitrago R, Cupolillo E, Bastrenta B, Le Pont F, Martinez E, Barnabe C,
Brenière SF (2011) PCR-RFLP of ribosomal internal transcribed spacers
highlights inter and intra-species variation among Leishmania strains
native to La Paz, Bolivia. Infect Genet Evol 11: 557-563.
38. Herrer A, Christensen HA, Beumer RJ (1973) Reservoir host of
cutaneous leishmaniasis among Panamanian forest mammals. Am J Trop
Med Hyg 22: 585-591.
39. Herrer A, Christensen HA (1976) Epidemiological patterns of cutaneous
leishmaniasis in Panama. III. Endemic persistence of the disease. Am J
Trop Med Hyg 25: 54-58.
40. Lima L, Silva FM, Neves L, Attias M, Takata CS, Campaner M, de Souza
W, Hamilton PB, Teixeira MM (2012) Evolutionary insights from bat
trypanosomes: morphological, developmental and phylogenetic evidence
of a new species, Trypanosoma (Schizotrypanum) erneyi sp. nov., in
African bats closely related to Trypanosoma (Schizotrypanum) cruzi and
allied species. Protist 163: 856-872.
41. Shapiro JT, da Costa Lima Jr MS, Dorval ME, de Oliveira FA, Cepa Matos
MF, Bordignon MO (2013) First record of Leishmania braziliensis
presence detected in bats, Mato Grosso do Sul, southwest Brazil. Acta
Trop 128: 171-174.
42. Falqueto A, Sessa PA, Varejão JBM, Barros GC, Momen H, Grimaldi Jr G
1991. Leishmaniasis due to Leishmania braziliensis in Espírito Santo
state, Brazil. Further evidence on the role of dogs as a reservoir of
infection for humans. Mem Inst Oswaldo Cruz 86: 499-500.
43. Dantas-Torres F (2007) e role of dogs as reservoirs of Leishmania
parasites, with emphasis on Leishmania (Leishmania) infantum and
Leishmania (Viannia) braziliensis. Vet Parasitol 149: 139-146.
44. Kent A, Ramkalup P, Mans D, Schallig H (2013) Is the dog a possible
reservoir for cutaneous leishmaniasis in suriname? J Trop Med 2013:
324140.
45. Baleela R, Llewellyn MS, Fitzpatrick S, Kuhls K, Schönian G, et al. (2014)
Leishmania donovani populations in Eastern Sudan: temporal structuring
and a link between human and canine transmission. Parasit Vectors 7:
496.
46. Cardoso L, Lopes AP, Sherry K, Schallig H, Solano-Gallego L (2010) Low
seroprevalence of Leishmania infantum infection in cats from northern
Portugal based on DAT and ELISA. Vet Parasitol 174: 37-42.
47. Maia C, Campino L (2011) Can domestic cats be considered reservoir
hosts of zoonotic leishmaniasis? Trends Parasitol 27: 341-344.
48. Lopes AP, Sousa S, Dubey JP, Ribeiro AJ, Silvestre R, Cotovio M, Schallig
HD, Cardoso L, Cordeiro-da-Silva A (2013) Prevalence of antibodies to
Leishmania infantum and Toxoplasma gondii in horses from the north of
Portugal. Parasit Vectors 6: 178.
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 11 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
49. Truppel JH, Otomura F, Teodoro U, Massafera R, Vieira da Costa-Ribeiro
MC, Catarino CM, Dalagrana L, Costa Ferreira ME, omaz-Soccol V
(2014) Can equids be a reservoir of Leishmania braziliensis in endemic
areas? PLoS ONE 9: e93731.
50. Killick-Kendrick R (1999) e biology and control of phlebotomine sand
ies. Clin Dermatol 17: 279-289.
51. Vannier-Santos MA, Martiny A, de Souza W (2002) Cell biology of
Leishmania spp.: invading and evading. Curr Pharm Des 8: 297-318.
52. Kamhawi S (2006) Phlebotomine sand ies and Leishmania parasites:
friends or foes? Trends Parasitol 22: 439-445.
53. Dostálová A, Volf P (2012) Leishmania development in sand ies:
parasite-vector interactions overview. Parasit Vectors 5: 276. DOI:
10.1186/1756-3305-5-276.
54. Reithinger R, Dujardin JC, Louzir H, Pirmez C, Alexander B, et al. (2007)
Cutaneous leishmaniasis. Lancet Infect Dis 7: 581-596.
55. Romero GA, Boelaert M (2010) Control of visceral leishmaniasis in latin
america-a systematic review. PLoS Negl Trop Dis 4: e584.
56. Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, den
Boer M (2012) WHO Leishmaniasis Control Team, 2012. Leishmaniasis
worldwide and global estimates of its incidence. PLoS One 7: e35671.
57. Mukhopadhyay D, Dalton JE2, Kaye PM3, Chatterjee M4 (2014) Post
kala-azar dermal leishmaniasis: an unresolved mystery. Trends Parasitol
30: 65-74.
58. Zijlstra EE, Musa AM, Khalil EA, el-Hassan IM, el-Hassan AM (2003)
Post-kala-azar dermal leishmaniasis. Lancet Infect Dis 3: 87-98.
59. Ramesh V, Mukherjee A (1995) Post-kala-azar dermal leishmaniasis. Int J
Dermatol 34: 85-91.
60. Ganguly S, Saha P, Chatterjee M, Roy S, Ghosh TK, Guha SK, Kundu PK,
Bera DK, Basu N, Maji AK (2015) PKDL - A silent parasite pool for
transmission of leishmaniasis in kala-azar endemic areas of Malda
District, West Bengal, India. PLoS Negl Trop Dis :e0004138.
61. Faber WR, Oskam L, van Gool T, Kroon NC, Knegt-Junk KJ, et al. (2003)
Value of diagnostic techniques for cutaneous leishmaniasis. J Am Acad
Dermatol 49: 70-74.
62. de Vries HJ, Reedijk SH, Schallig HD (2015) Cutaneous leishmaniasis:
recent developments in diagnosis and management. Am J Clin Dermatol
16: 99-109.
63. Handler MZ, Patel PA, Kapila R, Al-Qubati Y, Schwartz RA (2015)
Cutaneous and mucocutaneous leishmaniasis: dierential diagnosis,
diagnosis, histopathology, and management. J Am Acad Dermatol 73:
911-926.
64. Sakkas H, Gartzonika C, Levidiotou S (2016) Laboratory diagnosis of
human visceral leishmaniasis. J Vector Borne Dis 53: 8-16.
65. Jha RK, Sah AK, Shah DK, Sah P (2013) e treatment of visceral
leishmaniasis: safety and ecacy. JNMA J Nepal Med Assoc 52: 645-651.
66. Boggild AK, Miranda-Verastegui C, Espinosa D, Arevalo J, Adaui V,
Tulliano G, Llanos-Cuentas A, Low DE (2007) Evaluation of a
microculture method for isolation of Leishmania parasites from
cutaneous lesions of patients in Peru. J Clin Microbiol 45: 3680-3684.
67. Chouihi E, Amri F, Bouslimi N, Siala E, Selmi K, et al. (2009) [Cultures
on NNN medium for the diagnosis of leishmaniasis]. Pathol Biol (Paris)
57: 219-224.
68. Weigle KA, Valderrama L, Arias AL, Santrich C, Saravia NG (1991)
Leishmanin skin test standardization and evaluation of safety, dose,
storage, longevity of reaction and sensitization. Am J Trop Med Hyg 44:
260-271.
69. Manzur A, Bari Au (2006) Sensitivity of leishmanin skin test in patients
of acute cutaneous leishmaniasis. Dermatol Online J 12: 2.
70. Akhoundi M, Downing T, Votýpka J, Kuhls K, Lukeš J, et al. (2017)
Leishmania infections: molecular targets and diagnosis. Mol Aspects
Med, pii: S0098-2997(16)30045-0.
71. Badaró R, Reed SG, Carvalho EM (1983) Immunouorescent antibody
test in American visceral leishmaniasis: sensitivity and specicity of
dierent morphological forms of two Leishmania species. Am J Trop Med
Hyg 32: 480-484.
72. Ryan JR, Smithyman AM, Rajasekariah GH, Hochberg L, Stiteler JM,
Martin SK (2002) Enzyme-linked immunosorbent assay based on soluble
promastigote antigen detects immunoglobulin M (IgM) and IgG
antibodies in sera from cases of visceral and cutaneous leishmaniasis. J
Clin Microbiol 40: 1037-1043.
73. Santos-Gomes G, Gomes-Pereira S, Campino L, Araujo MD, Abranches P
(2000) Performance of immunoblotting in diagnosis of visceral
leishmaniasis in human immunodeciency virus-Leishmania sp.-
coinfected patients. J Clin Microbiol 38: 175-178.
74. Gao CH, Yang YT, Shi F, Wang JY, Steverding D, et al. (2015)
Development of an Immunochromatographic Test for Diagnosis of
Visceral Leishmaniasis Based on Detection of a Circulating Antigen. PLoS
Negl Trop Dis 9: e0003902.
75. Oskam L, Nieuwenhuijs J, Hailu A (1999) Evaluation of the direct
agglutination test (DAT) using freeze-dried antigen for the detection of
anti-Leishmania antibodies in stored sera from various patient groups in
Ethiopia. Trans R Soc Trop Med Hyg 93: 275-277.
76. Chappuis F, Rijal S, Soto A, Menten J, Boelaert M (2006) A meta-analysis
of the diagnostic performance of the direct agglutination test and rK39
dipstick for visceral leishmaniasis. BMJ 333: 723.
77. Smyth AJ, Ghosh A, Hassan MQ, Basu D, De Bruijn MH, Adhya S, Mallik
KK, Barker DC (1992) Rapid and sensitive detection of Leishmania
kinetoplast DNA from spleen and blood samples of kala-azar patients.
Parasitol 105: 183-192.
78. Katakura K, Kawazu S, Naya T, Nagakura K, Ito M, et al. (1998) Diagnosis
of kala-azar by nested PCR based on amplication of the Leishmania
mini-exon gene. J Clin Microbiol 36: 2173-2177.
79. Van der Meide W, Guerra J, Schoone G, Farenhorst M, Coelho L, Faber
W, Peekel I, Schallig H (2008) Comparison between quantitative nucleic
acid sequence-based amplication, real-time reverse transcriptase PCR,
and real-time PCR for quantication of Leishmania parasites. J Clin
Microbiol 46: 73-78.
80. Van der Meide WF, Schoone GJ, Faber WR, Zeegelaar JE, de Vries HJ,
Ozbel Y, Lai A Fat RF, Coelho LI, Kassi M, Schallig HD (2005)
Quantitative nucleic acid sequence-based assay as a new molecular tool
for detection and quantication of Leishmania parasites in skin biopsy
samples. J Clin Microbiol 43: 5560-5566.
81. Mugasa CM, Laurent T, Schoone GJ, Basiye FL, Saad AA, El Sa S, Kager
PA, Schallig HD (2010) Simplied molecular detection of Leishmania
parasites in various clinical samples from patients with leishmaniasis.
Parasit Vectors 3: 13. DOI: 10.1186/1756-3305-3-13.
82. Adams ER, Schoone GJ, Ageed AF, Sa SE, Schallig HD. Development of
a reverse transcriptase loop-mediated isothermal amplication (LAMP)
assay for the sensitive detection of Leishmania parasites in clinical
samples (2010) Am J Trop Med Hyg 82: 591-596.
83. Van der Snoek EM, Lammers AM, Kortbeek LM, Roelfsema JH, Bart A,
Jaspers CA (2009) Spontaneous cure of American cutaneous
leishmaniasis due to Leishmania nai in two Dutch infantry soldiers.
Clin Exp Dermatol 34: e889-891.
84. Cota GF, de Sousa MR, Fereguetti TO, Saleme PS, Alvarisa TK, Rabello A
(2016) e cure rate aer placebo or no therapy in American cutaneous
leishmaniasis: a systematic review and meta-analysis. PLoS One 11:
e0149697.
85. Sundar S, Chakravarty J (2015) An update on pharmacotherapy for
leishmaniasis. Expert Opin Pharmacother 16: 237-252.
86. Hodiamont CJ, Kager PA, Bart A, de Vries HJ, van iel PP, Leenstra T, de
Vries PJ, van Vugt M, Grobusch MP, van Gool T (2014) Species-directed
therapy for leishmaniasis in returning travellers: a comprehensive guide.
PLoS Negl Trop Dis 8: e2832.
87. Gupta G, Oghumu S, Satoskar AR (2013) Mechanisms of immune
evasion in leishmaniasis. Adv Appl Microbiol 82: 155-184.
88. Sundar S, Singh A (2016) Recent developments and future prospects in
the treatment of visceral leishmaniasis. er Adv Infect Dis 3: 98-109.
89. El Darouti MA, Al Rubaie SM (1990) Cutaneous leishmaniasis.
Treatment with combined cryotherapy and intralesional stibogluconate
injection. Int J Dermatol 29: 56-59.
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 12 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
90. Salmanpour R, Razmavar MR, Abtahi N (2006) Comparison of
intralesional meglumine antimoniate, cryotherapy and their combination
in the treatment of cutaneous leishmaniasis. Int J Dermatol 45:
1115-1116.
91. Reithinger R, Mohsen M, Wahid M, Bismullah M, Quinnell RJ, Davies
CR, Kolaczinski J, David JR (2005) Ecacy of thermotherapy to treat
cutaneous leishmaniasis caused by Leishmania tropica in Kabul,
Afghanistan: a randomized, controlled trial. Clin Infect Dis 40:
1148-1155.
92. Aronson NE, Wortmann GW, Byrne WR, Howard RS, Bernstein WB, et
al. (2010) A randomized controlled trial of local heat therapy versus
intravenous sodium stibogluconate for the treatment of cutaneous
Leishmania major infection. PLoS Negl Trop Dis 4: e628.
93. Alkhawajah AM, Larbi E, Al-Gindan Y, Abahussein A, Jain S (1997)
Treatment of cutaneous leishmaniasis with antimony: intra-muscular
versus intralesional administration. Ann Trop Med Parasitol 91: 899-905.
94. Uzun S, Durdu M, Culha G, Allahverdiyev AM, Memisoglu HR (2004)
Clinical features, epidemiology, and ecacy and safety of intralesional
antimony treatment of cutaneous leishmaniasis: recent experience in
Turkey. J Parasitol 90: 853-859.
95. Asilian A, Jalayer T, Nilforooshzadeh M, Ghassemi RL, Peto R, et al.
(2003) Treatment of cutaneous leishmaniasis with aminosidine
(paromomycin) ointment: double-blind, randomized trial in the Islamic
Republic of Iran. Bull WHO 81: 353-359.
96. Armijos RX, Weigel MM, Calvopina M, Mancheno M, Rodriguez R
(2004) Comparison of the eectiveness of two topical paromomycin
treatments versus meglumine antimoniate for New World cutaneous
leishmaniasis. Acta Trop 91: 153-160.
97. Minodier P, Parola P (2007) Cutaneous leishmaniasis treatment. Travel
Med Infect Dis 5: 150-158.
98. Velasco-Castrejon O, Walton BC, Rivas-Sanchez B, Garcia MF, Lazaro GJ,
et al. (1997) Treatment of cutaneous leishmaniasis with localized current
eld (radio frequency) in Tabasco, Mexico. Am J Trop Med Hyg 57:
309-312.
99. Pratlong F, Deniau M, Darie H, Eichenlaub S, Pröll S, et al. (2002) Human
cutaneous leishmaniasis caused by Leishmania nai is wide-spread in
South America. Ann Trop Med Parasitol 96: 781-785.
100. Soto J, Rea J, Balderrama M, Toledo J, Soto P, et al. (2008) Ecacy of
miltefosine for Bolivian cutaneous leishmaniasis. Am J Trop Med Hyg 78:
210-211.
101. Machado PR, Ampuero J, Guimarães LH, Villasboas L, Rocha AT, et al.
(2010) Miltefosine in the treatment of cutaneous leishmaniasis caused by
Leishmania braziliensis in Brazil: a randomized and controlled trial. PLoS
Negl Trop Dis 4: e912.
102. Chrusciak-Talhari A, Dietze R, Chrusciak Talhari C, da Silva RM,
Gadelha Yamashita EP, et al. (2011) Randomized controlled clinical trial
to access ecacy and safety of miltefosine in the treatment of cutaneous
leishmaniasis caused by Leishmania (Viannia) guyanensis in Manaus,
Brazil. Am J Trop Med Hyg 84: 255-260.
103. Escobar P, Matu S, Marques C, Cro SL (2002) Sensitivities of Leishmania
species to hexadecylphosphocholine (miltefosine), ET-18-OCH(3)
(edelfosine) and amphotericin B. Acta Trop 81: 151-157.
104. Amato VS, Tuon FF, Imamura R, Abegao de Camargo R, Duarte MI, Neto
VA (2009) Mucosal leishmaniasis: description of case management
approaches and analysis of risk factors for treatment failure in a cohort of
140 patients in Brazil. JEADV 23: 1026-1034.
105. Mohebali M, Fotouhi A, Hooshmand B, Zarei Z, Akhoundi B, et al.
(2007) Comparison of miltefosine and meglumine antimoniate for the
treatment of zoonotic cutaneous leishmaniasis (ZCL) by a randomized
clinical trial in Iran. Acta Trop 103: 33-40.
106. van iel PP, Leenstra T, Kager PA, de Vries HJ, van Vugt M, et al. (2010)
Miltefosine treatment of Leishmania major infection: an observational
study involving Dutch military personnel returning from northern
Afghanistan. Clin Infect Dis 50: 80-83.
107. Robledo SM, Puerta JA, Muñoz DL, Guardo M, Vélez ID (2006) [Ecacy
and tolerance of pentamidine for treatment of cutaneous leishmaniasis
caused by por L. (V) panamensis in Colombia]. Biomedica 26: 188-193.
108. Fagundes-Silva GA, Romero GA, Cupolillo E, Yamashita EP, Gomes-Silva
A1, et al. (2015) Leishmania (Viannia) nai: rare enough to be neglected?
Mem Inst Oswaldo Cruz 110: 797-800.
109. Lai A Fat EJ, Vrede MA, Soetosenojo RM, Lai A Fat RF (2002)
Pentamidine, the drug of choice for the treatment of cutaneous
leishmaniasis in Surinam. Int J Dermatol 41: 796-800.
110. Blum JA, Hatz CF (2009) Treatment of cutaneous leishmaniasis in
travelers 2009. J Travel Med 16: 123-131.
111. van der Meide WF, Sabajo LO, Jensema AJ, Peekel I, Faber WR, et al.
(2009) Evaluation of treatment with pentamidine for cutaneous
leishmaniasis in Suriname. Int J Dermatol 48: 52-58.
112. Mans DR, Kent AD, Hu RV, Lai A Fat EJ, Schoone GJ, et al. (2015)
Monitoring the response of patients with cutaneous leishmaniasis to
treatment with pentamidine isethionate by quantitative real-time PCR,
and identication of Leishmania parasites not responding to therapy. Clin
Exp Dermatol 41: 610-615.
113. Sundar S, More DK, Singh MK, Singh VP, Sharma S, et al. (2000) Failure
of pentavalent antimony in visceral leishmaniasis in India: report from
the center of the Indian epidemic. Clin Infect Dis 31: 1104-1107.
114. Sundar S, Pai K, Kumar R, Pathak-Tripathi K, Gam AA, et al. (2001)
Resistance to treatment in Kala-azar: speciation of isolates from northeast
India. Am J Trop Med Hyg 65: 193-196.
115. Singh R, Kumar D, Ramesh V, Negi NS, Singh S, Salotra P (2006) Visceral
leishmaniasis, or Kala Azar (KA): high incidence of refractoriness to
antimony is contributed by anthroponotic transmission via post-KA
dermal leishmaniasis. J Infect Dis 194: 302-306.
116. Abdo MG, Elamin WM, Khalil EAG, Mukhtar MM (2003) Antimony-
resistant Leishmania donovani in eastern Sudan: incidence and in vitro
correlation. East Mediterr Health J 9: 837-843.
117. Sundar S, Rai M (2002) Advances in the treatment of leishmaniasis. Curr
Opin Infect Dis 15: 593-598.
118. Berman JD, Badaro R, akur CP, Wasunna KM, Behbehani K, Davidson
R, Kuzoe F, Pang L, Weerasuriya K, Bryceson AD (1998) Ecacy and
safety of liposomal amphotericin B (AmBisome) for visceral
leishmaniasis in endemic developing countries. Bull World Health Organ
76: 25-32.
119. Sundar S, Mehta H, Suresh AV, Singh SP, Rai M, Murray HW (2004)
Amphotericin B treatment for Indian visceral leishmaniasis: conventional
versus lipid formulations. Clin Infect Dis 38: 377-383.
120. Torchilin VP1 (2005) Lipid-core micelles for targeted drug delivery. Curr
Drug Deliv 2: 319-327.
121. Sundar S, Chakravarty J, Agarwal D, Rai M, Murray HW (2010) Single-
dose liposomal amphotericin B for visceral leishmaniasis in India. N Engl
J Med 362: 504-512.
122. Freire M, Badaró F, Avelar ME, Luz K, Nakatani MS, et al. (1997) Ecacy
and tolerability of liposomal amphotericin B (AmBisome) in the
treatment of visceral leishmaniasis in Brazil. Braz J Infect Dis 1: 230-240.
123. Syriopoulou V, Daikos GL, eodoridou M, Pavlopoulou I, Manolaki AG,
et al. (2003) Two doses of a lipid formulation of amphotericin B for the
treatment of Mediterranean visceral leishmaniasis. Clin Infect Dis 36:
560-566.
124. Bern C, Adler-Moore J, Berenguer J, Boelaert M, den Boer M, et al.
(2006) Liposomal amphotericin B for the treatment of visceral
leishmaniasis. Clin Infect Dis 43: 917-924.
125. Salih NA, van Griensven J, Chappuis F, Antierens A, Mumina A, et al.
(2014) Liposomal amphotericin B for complicated visceral leishmaniasis
(kala-azar) in Eastern Sudan: how eective is treatment for this neglected
disease? Trop Med Int Health 19: 146–152.
126. Cascio A, Colomba C (2003) [Childhood Mediterranean visceral
leishmaniasis]. Infez Med 11: 5-10.
127. Berman J (2005) Miltefosine to treat leishmaniasis. Expert Opin
Pharmacother 6: 1381-1388.
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 13 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
128. Sundar S, Jha TK, akur CP, Engel J, Sindermann H, et al. (2002) Oral
miltefosine for Indian visceral leishmaniasis. N Engl J Med 347:
1739-1746.
129. Bhattacharya SK, Jha TK, Sundar S, akur CP, Engel J, et al. (2004)
Ecacy and tolerability of miltefosine for childhood visceral
leishmaniasis in India. Clin Infect Dis 38: 217-221.
130. Ramesh V, Katara GK, Verma S, Salotra P (2011) Miltefosine as an
eective choice in the treatment of post-kala-azar dermal leishmaniasis.
Br J Dermatol 165: 411-414.
131. Sundar S, Sinha P, Jha TK, Chakravarty J, Rai M, Kumar N, Pandey K,
Narain MK, Verma N, Das VN, Das P, Berman J, Arana B (2013) Oral
miltefosine for Indian post-kala-azar dermal leishmaniasis: a randomised
trial. Trop Med Int Health 18: 96-100.
132. Sundar S, Olliaro PL (2007) Miltefosine in the treatment of leishmaniasis:
Clinical evidence for informed clinical risk management. er Clin Risk
Manag 3: 733-740.
133. Seifert K, Cro SL (2006) In vitro and in vivo interactions between
miltefosine and other antileishmanial drugs. Antimicrob Agents
Chemother 50: 73-79.
134. Sundar S, Jha TK, akur CP, Sinha PK, Bhattacharya SK (2007)
Injectable paromomycin for Visceral leishmaniasis in India. N Engl J Med
356: 2571-2581.
135. Chunge CN, Owate J, Pamba HO, Donno L (1990) Treatment of visceral
leishmaniasis in Kenya by aminosidine alone or combined with sodium
stibogluconate. Trans R Soc Trop Med Hyg 84: 221-225.
136. akur CP, Olliaro P, Gothoskar S, Bhowmick S, Choudhury BK, et al.
(1992) Treatment of visceral leishmaniasis (kala-azar) with aminosidine
(= paromomycin)-antimonial combinations, a pilot study in Bihar, India.
Trans R Soc Trop Med Hyg 86: 615-616.
137. Seaman J, Pryce D, Sondorp HE, Moody A, Bryceson AD, Davidson RN
(1993) Epidemic visceral leishmaniasis in Sudan: a randomized trial of
aminosidine plus sodium stibogluconate versus sodium stibogluconate
alone. J Infect Dis 168: 715-720.
138. akur CP, Bhowmick S, Dol L, Olliaro P (1995) Aminosidine plus
sodium stibogluconate for the treatment of Indian kala-azar: a
randomized dose-nding clinical trial. Trans R Soc Trop Med Hyg 89:
219-223.
139. Sundar S, Rai M (2005) Treatment of visceral leishmaniasis. Expert Opin
Pharmacother 6: 2821-2829.
140. Sundar S, Chakravarty J (2013) Leishmaniasis: an update of current
pharmacotherapy. Expert Opin Pharmacother 14: 53-63.
141. Singh OP, Singh B, Chakravarty J, Sundar S (2016) Current challenges in
treatment options for visceral leishmaniasis in India: a public health
perspective. Infect Dis Poverty 5: 19.
142. Ouellette M, Drummelsmith J, Papadopoulou B (2004) Leishmaniasis:
drugs in the clinic, resistance and new developments. Drug Resist Updat
7: 257-266.
143. Jha SN, Singh NK, Jha TK (1991) Changing response to diamidine
compounds in cases of kala-azar unresponsive to antimonial. J Assoc
Physicians India 39: 314-316.
144. Cro SL, Coombs GH (2003) Leishmaniasis--current chemotherapy and
recent advances in the search for novel drugs. Trends Parasitol 19:
502-508.
145. Otranto D, Dantas-Torres F (2013) e prevention of canine
leishmaniasis and its impact on public health. Trends Parasitol 29:
339-345.
146. Costa CH (2011) How eective is dog culling in controlling zoonotic
visceral leishmaniasis? A critical evaluation of the science, politics and
ethics behind this public health policy. Rev Soc Bras Med Trop 44:
232-242.
147. Debboun M, Strickman D (2013) Insect repellents and associated
personal protection for a reduction in human disease. Med Vet Entomol
27: 1-9.
148. Banks SD, Murray N, Wilder-Smith A, Logan JG (2014) Insecticide-
treated clothes for the control of vector-borne diseases: a review on
eectiveness and safety. Med Vet Entomol 28 :14-25.
149. Kitchen LW, Lawrence KL, Coleman RE (2009) e role of the United
States military in the development of vector control products, including
insect repellents, insecticides, and bed nets. J Vector Ecol 34: 50-61.
150. Bakker E, Dalhuisen L, Donk R, Hassankhan M, Steegh F (1998)
Geschiedenis van Suriname: van stam tot staat (History of Suriname:
from tribe to state). Zutphen: Walburg Pers.
151. Algemeen Bureau voor de Statistiek/Conservation International
Suriname. Suriname in cijfers 286-2012/04. (General Bureau of Statistics/
Conservation International Suriname. Suriname in numbers
286-2012/04). Milieustatistieken (Environment Statistics). Paramaribo:
Algemeen Bureau voor de Statistiek; 2012.
152. Algemeen Bureau voor de Statistiek/Censuskantoor. Suriname in cijfers
2013/05. Resultaten achtste (8ste) volks- en woningtelling in Suriname
(volume 1) (General Bureau of Statistics/Census oce. Suriname in
numbers 2013/05. Results of the eight general census of Suriname).
Demograsche en sociale karakteristieken en migratie (Demographic and
social characteristics and migration). Paramaribo: Algemeen Bureau voor
de Statistiek; 2013.
153. Davidson EA, de Araújo AC, Artaxo P, Balch JK, Brown IF, et al. (2012)
e Amazon basin in transition. Nature 481: 321-328.
154. Hammond DS (2005) Forest conservation and management in the
Guiana Shield (Chapter 1). In: Hammond DS, editor. Tropical rainforests
of the Guiana shield. Wallingford: CABI Publishing: 1–14.
155. Algemeen Bureau voor de Statistiek. Suriname in cijfers 303-2014-04
(General Bureau of Statistics. Suriname in numbers 303-2014-04). Basis
indicatoren (Basic indicators). Paramaribo: Algemeen Bureau voor de
Statistiek; 2014.
156. e World Bank. Suriname overview [Internet]. 2014.
157. Ministry of Health (2008) Report of the Director of Health 2005-2007.
Ministry of Health Republic of Suriname, Paramaribo.
158. van der Meide WF, Jensema AJ, Akrum RA, Sabajo LO, Lai A Fat RF, et
al. (2008) Epidemiology of cutaneous leishmaniasis in Suriname: a study
performed in 2006. Am J Trop Med Hyg 79: 192-197.
159. Flu PC (1911) Die aetiologie der in Surinam vorkommenden
sogenannten “Boschyaws,” einer der Aleppobeule analogen Erkrankung.
Zentralblatt für Bakteriologie und Parasitenkunde 60: 624-637.
160. Mans DRA, Kent AD, Schallig HDFH (2016) ‘Aleppo evil’, ‘white leprosy’,
‘busi yasi’: biological and clinical aspects of cutaneous leishmaniasis with
new insights from Suriname. J Drug Des Res 3 : 1020.
161. Ramdas S (2012) Cruel disease, cruel medicine: self-treatment of
cutaneous leishmaniasis with harmful chemical substances in Suriname.
Soc Sci Med 75: 1097-1105.
162. Ramdas S, van der Geest S2, Schallig HD3 (2016) Nuancing stigma
through ethnography: the case of cutaneous leishmaniasis in Suriname.
Soc Sci Med 151: 139-146.
163. van iel PP, Gool Tv, Kager PA, Bart A (2010) First cases of cutaneous
leishmaniasis caused by Leishmania (Viannia) nai infection in Surinam.
Am J Trop Med Hyg 82: 588-590.
164. Hu RVPF, Straetemans M, Kent AD, Sabajo LOA, de Vries HJC, Lai A Fat
RFM (2015) Randomized single-blinded non-inferiority trial of 7 mg/kg
pentamidine isethionate versus 4 mg/kg pentamidine isethionate for
cutaneous leishmaniaisis in Suriname. PLoS Negl Trop Dis 9: e0003592.
165. Van der Meide WF, de Vries HJC, Pratlong F, van der Wal A, Sabajo LOA
(2008) First reported case of disseminated cutaneous leishmaniasis
caused by Leishmania (Leishmania) amazonensis infection, Suriname.
Emerg Inf Dis 14: 857-859.
166. Burgos A, Hudson J (1994) Annotated list of the phlebotominae (Diptera)
of Suriname. Mem Inst Oswaldo Cruz 89: 171-178.
167. Kent AD, Dos Santos TV, Gangadin A, Samjhawan A, Mans DRA,
Schallig HDFH (2013) Studies on the sand y fauna (Diptera:
Psychodidae) in high-transmission areas of cutaneous leishmaniasis in
the Republic of Suriname. Parasit Vectors 6: 318.
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 14 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
168. Grimaldi G Jr, Tesh RB, McMahon-Pratt D (1989) A review of the
geographic distribution and epidemiology of leishmaniasis in the New
World. Am J Trop Med Hyg 41: 687-725.
169. Weigle KA, Santrich C, Martinez F, Valderrama L, Saravia NG (1993)
Epidemiology of cutaneous leishmaniasis in Colombia: environmental
and behavioral risk factors for infection, clinical manifestations, and
pathogenicity. J Infect Dis 168: 709-714.
170. Mouchet J, Le Pont F, Leon R, Echeverria R, Guderian RH (1994)
[Leishmaniasis in Ecuador. 5. Leishmaniasis and anthropization on the
Pacic coast]. Ann Soc Belg Med Trop 74: 35-41.
171. Lucas CM1, Franke ED, Cachay MI, Tejada A, Cruz ME, et al. (1998)
Geographic distribution and clinical description of leishmaniasis cases in
Peru. Am J Trop Med Hyg 59: 312-317.
172. Lainson R, Shaw JJ (2005) New World leishmaniasis. In: Cox FEG,
Wakelin D, Gillespie SH, Despommier DD, eds. Topley and Wilson’s
Microbiology and Microbial Infections, Parasitology. 10th ed. ASM Press,
London, p. 313-349.
173. Rodríguez-Barraquer I, Góngora R, Prager M, Pacheco R, Montero LM,
et al. (2008) Etiologic agent of an epidemic of cutaneous leishmaniasis in
Tolima, Colombia. Am J Trop Med Hyg 78: 276-282.
174. Córdova O, Vargas F, Hashiguchi Y, Kato H, Gómez E (2011)
Identicación de species de Leishmania en pacientes y ebotominos en
áreas de transmisión en una región de Perú. Revista Peruana de Medicina
Experimental y Salud Pública 28: 446-453.
175. Guerra JA, Prestes SR, Silveira H, Coelho L, Gama P, Moura A, Amato V,
Barbosa Md, Ferreira LC (2011) Mucosal leishmaniasis caused by
Leishmania (Viannia) braziliensis and Leishmania (Viannia) guyanensis
in the Brazilian Amazon. PLoS Negl Trop Dis 5: e980.
176. Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L (2013)
Phlebotomine sandies and the spreading of leishmaniases and other
diseases of public health concern. Med Vet Entomol 27: 123-147.
177. Feliciangeli MD, Rodriguez N, Bravo A, Arias F, Guzman B (1994)
Vectors of cutaneous leishmaniasis in north-central Venezuela. Med Vet
Entomol 8: 317-324.
178. Freitas RA, Nai RD, Barrett TV (2002) Species diversity and agellate
infections in the sand y fauna near Porto Grande, state of Amapá, Brazil
(Diptera: Psychodidae. Kinetoplastida: Trypanosomatidae). Mem Inst
Oswaldo Cruz 97: 53-59.
179. Santaella J1, Ocampo CB, Saravia NG, Méndez F, Góngora R, et al. (2011)
Leishmania (Viannia) infection in the domestic dog in Chaparral,
Colombia. Am J Trop Med Hyg 84: 674-680.
180. Vélez ID, Carrillo LM, López L, Rodríguez E, Robledo SM (2012) An
epidemic outbreak of canine cutaneous leishmaniasis in Colombia caused
by Leishmania braziliensis and Leishmania panamensis. Am J Trop Med
Hyg 86: 807-811.
181. Shaw JJ (1992) Endotrypanum, a unique intraerythrocytic agellate of
New World tree sloths. An evolutionary link or an evolutionary
backwater? Ciência e Cultura. Rio de janeiro 44: 107-116.
182. Rotureau B1, Gaborit P, Issaly J, Carinci R, Fouque F, et al. (2006)
Diversity and ecology of sand ies (Diptera: Psychodidae:
Phlebotominae) in coastal French Guiana. Am J Trop Med Hyg 75: 62-69.
183. Moreira CR, Rebelo JM, Gama ME, Costa JM (2002) Knowledge level
about American tugementary leishmaniasis (ATL) and use of alternative
therapies in an endemic area in the Amazon region in the State of
Maranhao, Brazil. Cad Saúde Pública 18: 187-195.
184. Cro SL, Yardley V, Kendrick H (2002) Drug sensitivity of Leishmania
species: some unresolved problems. Trans R Soc Trop Med Hyg 96 Suppl
1: S127-129.
185. Cro SL, Sundar S, Fairlamb AH (2006) Drug resistance in leishmaniasis.
Clin Microbiol Rev 19: 111-126.
186. Silveira FT, Shaw JJ, Braga RR, Ishikawa E (1987) Dermal leishmaniasis in
the Amazon region of Brazil: Leishmania (Viannaia) lainsoni sp.n., a new
parasite from the State of Pará. Mem Inst Oswaldo Cruz 82: 289-291.
187. Tojal da Silva AC, Cupolillo E, Volpini AC, Almeida R, Romero GA
(2006) Species diversity causing human cutaneous leishmaniasis in Rio
Branco, state of Acre, Brazil. Trop Med Int Health 11: 1388-1398.
188. Lucas CM, Franke ED, Cachay MI, Tejada A, Carrizales D, et al. (1994)
Leishmania (Viannia) lainsoni: rst isolation in Peru. Am J Trop Med
Hyg 51: 533-537.
189. Martinez E1, Le Pont F, Mollinedo S, Cupolillo E (2001) A rst case of
cutaneous leishmaniasis due to Leishmania (Viannia) lainsoni in Bolivia.
Trans R Soc Trop Med Hyg 95: 375-377.
190. Bastrenta B, Buitrago R, Vargas F, Le Pont F, Torrez M, et al. (2002) First
evidence of transmission of Leishmania (Viannia) lainsoni in a Sub
Andean region of Bolivia. Acta Tropica 83: 249-253.
191. Kato H, Gomez EA, Martini-Robles L, Muzzio J, Velez L, et al. (2016)
Geographic distribution of Leishmania species in Ecuador based on the
cytochrome b gene sequence analysis. PLoS Negl Trop Dis. 2016 Jul
13;10 :e0004844.
192. Silveira FT, Souza AAA, Lainson R, Shaw JJ, Braga RR, Ishikawa EA
(1991) Cutaneous leishmaniasis in the Amazon region: natural infection
of the sandy Lutzomyia ubiquitalis (Psychodidae: Phlebotominae) by
Leishmania (Viannia) lainsoni in Pará state, Brazil. Mem Inst Oswaldo
Cruz 86: 127-130.
193. Lainson R, Shaw JJ, Souza AAA, Silveira FT, Falqueto A (1992) Further
observations on Lutzomyia ubiquitalis (Psychodidae: Phlebotominae), the
sandy vector of Leishmania (Viannia) lainsoni. Mem Inst Oswaldo Cruz
87: 437-439.
194. Azevedo ACR, Costa SM, Pinto MC, Souza JL, Cruz HC, et al. (2008)
Studies on the sandy fauna (Diptera: Psychodidae: Phlebotominae) from
transmission areas of American cutaneous leishmaniasis in state of Acre,
Brazil. Mem Inst Oswaldo Cruz 103: 760-767.
195. Torrez M, Lopez M, Le Pont F, Martinez E, Muñoz M, Hervas D, et al.
(1998) Lutzomyia nuneztovari anglesi (Diptera: Psychodidae) as a
probable vector of Leishmania braziliensis in the Yungas, Bolivia. Acta
Trop 71: 311-316.
196. BRUIJNING CF (1957) Man-biting sandies (Phlebotomus) in the
endemic leishmaniasis area of Surinam. Doc Med Geogr Trop 9: 229-236.
197. Rangel EF, Lainson R (2009) Proven and putative vectors of American
cutaneous leishmaniasis in Brazil: aspects of their biology and vectorial
competence. Mem Inst O Cruz 104: 937-954.
198. Arias JR, Miles MA, Nai RD, Povoa MM, de Freitas RA, et al. (1985)
Flagellate infections of Brazilian sand ies (Diptera: Psychodidae):
isolation in vitro and biochemical identication of Endotrypanum and
Leishmania. Am J Trop Med Hyg 34: 1098-1108.
199. Lainson R, Shaw JJ, Silveira FT, Braga RR, Ishikawa EA (1990) Cutaneous
leishmaniasis of man due to Leishmania (Viannia) nai Lainson and
Shaw, 1989. Ann Parasitol Hum Comp 65: 282-284.
200. Gil LH, Basano SA, Souza AA, Silva MG, Barata I, et al. (2003) Recent
observations on the sandy (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 98: 751-755.
201. Kato H, Gomez EA, Yamamoto Y, Calvopiña M, Guevara AG, et al.
(2008) Natural infection of Lutzomyia tortura with Leishmania (Viannia)
nai in an Amazonian area of Ecuador. Am J Trop Med Hyg 79: 438-440.
202. Felinto de Brito ME, Andrade MS, de Almeida EL, Medeiros AC,
Werkhäuser RP, et al. (2012) Occupationally acquired American
cutaneous leishmaniasis. Case Rep Dermatol Med 2012: 279517.
203. Darie H, Deniau M, Pratlong F, Lanotte G, Talarmin A, et al. (1995)
Cutaneous leishmaniasis of humans due to Leishmania (Viannia) nai
outside Brazil. Trans R Soc Trop Med Hyg 89: 476-477.
204. Kato H, Calvopiña M, Criollo H, Hashiguchi Y (2013) First human cases
of Leishmania (Viannia) nai infection in Ecuador and identication of
its suspected vector species. Acta Trop 128:710-713.
205. Jones TC, Johnson WD Jr, Bareto AC, Lago E, Badaro R, et al. (1987)
Epidemiology of American cutaneous leishmaniasis due to Leishmania
braziliensis braziliensis. J Infect Dis 156: 73-83.
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 15 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
206. Passos VMA, Fernandes O, Lacerda PAF, Volpini AC, Gontijo CMF, et al.
(1999) Leishmania (Viannia) braziliensis is the predominant specie
infecting patients with American cutaneous leishmaniasis in the State of
Minas Gerais, southeast Brazil. Acta Tropica 72: 251-258.
207. Lainson R (1985) Our present knowledge of the ecology and control of
leishmaniasis in the Amazon Region of Brazil. Rev Soc Bras Med Trop 18:
47-56.
208. Amato VS, Tuon FF, Siqueira AM, Nicodemo AC, Neto VA (2007)
Treatment of mucosal leishmaniasis in Latin America: systematic review.
Am J Trop Med Hyg 77: 266-274.
209. Odiwuor S, Veland N, Maes I, Arevalo J, Dujardin JC, et al. Evolution of
the Leishmania braziliensis species complex from amplied fragment
length polymorphisms, and clinical implications. Infect Genet Evol 12:
1994-2002.
210. Lainson R, Shaw JJ, Ward RD, Fraiha H (1973) Leishmaniasis in Bazil. IX.
Considerations on the Leishmania braziliensis complex: importance of
sandies of the genus Psychodopygus (Mangabeira) in the transmission
of L. braziliensis braziliensis in north Brazil. Trans R Soc Trop Med Hyg
67: 184-196.
211. De Queiroz RG, Vasconcelos Ide A, Vasconcelos AW, Pessoa FA, de Sousa
RN, et al. (1994) Cutaneous leishmaniasis in Ceara state in northeastern
Brazil: incrimination of Lutzomyia whitmani (Diptera: Psychodidae) as a
vector of Leishmania braziliensis in Baturité municipality. Am J Trop
Med Hyg 50: 693-698.
212. Luz E, Membrive N, Castro EA, Dereure J, Pratlong F, et al. (2000)
Lutzomyia whitmani (Diptera: Psychodidae) as vector of Leishmania (V.)
braziliensis in Paraná state, southern Brazil. Ann Trop Med Parasitol 94:
623-631.
213. Pita-Pereira D, Alves CR, Souza MB, Brazil RP, Bertho A, et al. (2005)
Identication of naturally infected Lutzomyia intermedia and Lutzomyia
migonei with Leishmania (Viannia) braziliensis in Rio de Janeiro Brazil
revealed by a PCR multiplex non-isotopic hybridization assay. Trans R
Soc Trop Med Hyg 99: 905-913.
214. Carvalho BM, Maximo M, Costa WA, de Santana AL, da Costa SM, et al.
(2013) Leishmaniasis transmission in an ecotourism area: potential
vectors in Ilha Grande, Rio de Janeiro State, Brazil. Parasit Vectors 6: 325.
215. Guimarães VCFV, Costa PL, Silva FJ, Melo FL, et al. (2014) Molecular
detection of Leishmania in phlebotomine sand ies in a cutaneous and
visceral leishmaniasis endemic area in northeastern Brazil. Rev Inst Med
Trop Sao Paulo 56: 357-360.
216. Rangel EF, de Souza NA, Wermelinger ED, Barbosa AF (1984) [Natural
infection of Lutzomyia intermedia Lutz & Neiva, 1912, in an endemic
area of visceral leishmaniasis of Rio de Janeiro]. Mem Inst Oswaldo Cruz
79: 395-396.
217. Mayo RC, Casanova C, Mascarini LM, Pignatti MG, Rangel O, et al.
(1998) Flebotomíneos (Diptera, Psychodidae) de área de transmissão de
leishmaniose tegumentar americana no município de Itaupeva, região
sudeste do estado de São Paulo, Brasil. Rev Soc Bras Med Trop 31:
339-345.
218. Ferreira AL, Sessa PA, Varejão JBM, Falqueto A (2001) Distribution of
sand ies (Diptera: Psychodidae) at dierent altitudes in an endemic
region of American cutaneous leishmaniasis in the state of Espírito Santo,
Brazil. Mem Inst Oswaldo Cruz 96: 1061-1067.
219. Falqueto A, Sessa PA, Ferreira AL, Vieira VP, Santos CB, et al. (2003)
Epidemiological and clinical features of Leishmania (Viannia) braziliensis
American cutaneous and mucocutaneous leishmaniasis in the State of
Espirito Santo, Brazil. Mem Inst Oswaldo Cruz 98: 1003-1010.
220. Grimaldi Jr G, David JR, McMahon-Pratt D (1987) Identication and
distribution of New World Leishmania species characterized by serademe
analysis using monoclonal antibodies. Am J Trop Med Hyg 36: 270-287.
221. Grisard EC, Steindel M, Shaw JJ, Ishikawa EAY, Carvalho-Pinto CJ, et al.
(2000) Characterization of Leishmania sp. strains isolated from
autochtonous cases of human cutaneous leishmaniasis in Santa Catarina
State, southern Brazil. Acta Tropica 74: 89-93, 2000.
222. Dorval MEMC, Oshiro ET, Cupollilo E, de Castro ACC, Alves TP (2006)
Ocorrência de leishmaniose tegumentar americana no Estado do Mato
Grosso do Sul associada à infecção por Leishmania (Leishmania)
amazonensis. Rev Soc Bras Med Trop 39: 43-46.
223. Camara Coelho LI1, Paes M, Guerra JA, Barbosa Md, Coelho C, et al.
(2011) Characterization of Leishmania spp. causing cutaneous
leishmaniasis in Manaus, Amazonas, Brazil. Parasitol Res 108: 671-677.
224. Bermudez H, Torrico F, Rojas E, Balderrama F, Le Ray D, et al. (1993)
Leishmaniasis in the lowlands of Bolivia, prevalence of the disease in two
groups of localities with dierent settlement ages in Carrasco Tropical,
Cochabamba. Archs Inst Pasteur Tunis 70: 443-453.
225. Martínez E1, Le Pont F, Torrez M, Tellería J, Vargas F, et al. (1998) A new
focus of cutaneous leishmaniasis due to Leishmania amazonensis in a Sub
Andean region of Bolivia. Acta Trop 71: 97-106.
226. Young D, Duncan M (1994) Guide to the identication and geographic
distribution of Lutzomyia sand ies in Mexico, the West Indies, Central
and South America (Diptera: Psychodidae). Mem Entomol Inst 54: 1-881.
227. Dorval ME, Alves TP, Cristaldo G, Rocha HC, Alves MA, et al. (2010)
Sandy captures with Disney traps in area of occurrence of Leishmania
(Leishmania) amazonensis in the state of Mato Grosso do Sul, mid-
western Brazil. Rev Soc Bras Med Trop 43: 491-495.
228. Lainson R, Ryan L, Shaw JJ (1987) Infective stages of Leishmania in the
sandy vector and some observations on the mechanism of transmission.
Mem Inst Oswaldo Cruz 82: 421-424.
229. Martinez E, LePont F, Torrez M, Telleria J, Vargas F, et al. (1999)
Lutzomyia nuneztovari anglesi (LesPont & Desjeuz, 1984) as a vector of
Leishmania amazonensis in a sub-Andean leishmaniasis focus of Bolivia.
Am J Trop Med Hyg 61: 846-849.
230. Telleria J, Bosseno MF, Tarifa T, Buitrago R, Martinez E, et al. (1999)
Putative reservoirs of Leishmania amazonensis in a Sub-andean focus of
Bolivia identied by kDNA-Polymerase Chain Reaction. Mem Inst
Oswaldo Cruz 94: 5-6.
231. Nieves E, Pimenta PF (2000) Development of Leishmania (Viannia)
braziliensis and Leishmania (Leishmania) amazonensis in the sandy
Lutzomyia migonei (Diptera: Psychodidae). J Med Entomol 37: 134-140.
232. Kerr SF, Emmons LH, Melby PC, Liu C, Perez LE, et al. (2006)
Leishmania amazonensis infections in Oryzomys acritus and Oryzomys
nitidus from Bolivia. Am J Trop Med Hyg 75: 1069-1073.
233. Homann AR, Navarro IT, Camargo Jr VE, Caldart ET, Regina Mitsuka
Breganó RM, et al. (2012) Leishmania amazonensis in dog with clinical
diagnosis of visceral leishmaniasis in Paraná State, Brazil - a case report.
Semina: Ciências Agrárias, Londrina 33: 3265-3270.
234. Silveira FT, Lainson R, Corbett CE (2005) Further observations on
clinical, histopathological, and immunological features of borderline
disseminated cutaneous leishmaniasis caused by Leishmania
(Leishmania) amazonensis. Mem Inst Oswaldo Cruz 100: 525-534.
235. Barral A, Pedral-Sampaio D, Grimaldi G, Momen H, McMahon-Pratt D,
et al. (1991) Leishmaniasis in Bahia, Brazil: evidence that Leishmania
amazonensis produces a wide spectrum of clinical disease. Am J Trop
Med Hyg 44: 536-546.
Citation: Mans DRA, Kent AD, Hu RVPF, Schallig HDFH (2017) Epidemiological, Biological and Clinical Aspects of Leishmaniasis with Special
Emphasis on Busi Yasi in Suriname. J Clin Exp Dermatol Res 8: 388. doi:10.4172/2155-9554.1000388
Page 16 of 16
J Clin Exp Dermatol Res, an open access journal
ISSN:2155-9554
Volume 8 • Issue 2 • 1000388
