DOI: 10.1590/S0037-86822011000500006
Revista da Sociedade Brasileira de Medicina Tropical 44(5):561-566, set-out, 2011
Article/Artigo
Epidemiological aspects of human and canine visceral leishmaniasis in
Montes Claros, State of Minas Gerais, Brazil, between 2007 and 2009
Aspectos epidemiológicos da leishmaniose visceral humana e canina em Montes Claros,
Estado de Minas Gerais, Brasil, entre 2007 e 2009
Patrícia Fernandes do Prado 1, Marília Fonseca Rocha 1,2, Joel Fontes de Sousa 2, Dênio Iuri Caldeira 2,
Gustavo Fontes Paz3 and Edelberto Santos Dias3
ABSTRACT
Introduction: Visceral leishmaniasis (VL) is an expanding zoonosis in Brazil and is becoming
urbanized in several Brazilian regions. This study aims to describe the epidemiological features
of human and canine VL in the municipality of Montes Claros, State of Minas Gerais, by
focusing on their spatial distribution. Methods: Data concerning human cases and reactive
dogs for VL from 2007 to 2009 were obtained from the Information System for Disease
Notification (SINAN) and from reports of the local Centro de Controle de Zoonoses (CCZ),
respectively. The addresses of human and canine cases have been georeferenced and localized
in thematic maps, allowing their spatial visualization as well as the identification of areas at risk
of VL transmission. Results: Ninety-five cases of human VL were reported in the period. The
0-9-year-old age group (48.4%) was the most affected, within which the majority consisted
of male patients (64%). Of the samples collected for the canine serological survey, 2,919
(6.3%) were reactive to VL. The spatial localization of these cases shows that the disease was
scattered in the urban area of the municipality. Areas showing a higher dissemination risk were
concentrated in the central, northwestern, and southern regions of the city. Conclusions:
Identifying the areas most at risk in urban Montes Claros may help guide actions toward local
epidemiological vigilance and control.
Keywords: Visceral leishmaniasis. Epidemiology. Spatial distribution.
RESUMO
Introdução: A leishmaniose visceral (LV) é uma zoonose em expansão no Brasil e está se
tornando urbana em várias regiões brasileiras. Este estudo descreve aspectos epidemiológicos
da LV humana e canina no município de Montes Claros, Minas Gerais, com enfoque na
distribuição espacial de sua incidência. Métodos: É um estudo epidemiológico descritivo,
que utiliza dados relativos à casos humanos e soro-positividade canina para LV, obtidos do
Sistema de Informação de Agravos de Notificação (SINAN) e de relatórios do Centro de
Controle de Zoonoses (CCZ) local. Os endereços dos casos estudados foram georreferenciados
e localizados em mapas temáticos que permitem sua visualização espacial, bem como a
identificação de áreas de risco de transmissão da doença. Resultados: A leishmaniose visceral
humana e canina mostrou ampla distribuição espacial em Montes Claros. No período entre
2007 a 2009, foram notificados 95 casos humanos da doença. O grupo etário entre 0 e 9
anos foi o mais afetado (48.4%) com maior prevalência no sexo masculino (64%). Dentre as
amostras caninas coletadas para investigação sorológica, 2.919 (6,3%) foram reativas para LV.
A localização espacial desses casos mostra que a doença está disseminada na área urbana do
município. As áreas com maior risco de disseminação concentraram-se nas regiões central,
noroeste e sul da cidade. Conclusões: A identificação das áreas de maior risco na zona urbana
de Montes Claros poderá guiar as ações de vigilância epidemiológica e de controle locais.
Palavras-chaves: Leishmaniose visceral. Epidemiologia. Distribuição espacial.
1. Programa de Pós-Graduação em Ciências da Saúde, Universidade Estadual de Montes Claros,
Montes Claros, MG. 2. Centro de Controle de Zoonoses, Secretaria Municipal de Saúde de Montes Claros,
Montes Claros, MG. 3. Laboratório de Leishmanioses, Centro de Pesquisas René Rachou, Fundação
Oswaldo Cruz, Belo Horizonte, MG.
Address to: Dr. Edelberto Santos Dias. Lab. Leishmanioses/CPqRR/FIOCRUZ. Av. Augusto de Lima 1715,
30190-002 Belo Horizonte, MG, Brasil.
Phone: 55 31 3349-7700; Fax: 55 31 3295-3115
e-mail: edel@cpqrr.fiocruz.br
Received in 28/01/2011
Accepted in 05/04/2011
INTRODUCTION
Visceral leishmaniasis (VL) is thoroughly
disseminated all over the world and is endemic in
approximately 72 countries1, mainly in the tropical and
subtropical regions of Asia, the Middle East, Africa,
Central America, and South America. The estimated
incidence of VL reaches 500,000 new cases annually2,
and the disease may turn into an anthroponosis or
anthropozoonosis when humans act as reservoirs. VL
is a systemic and serious disease that can affect children,
youth, adults, and immunodepressed persons. It is
characterized by long-lasting fever and other symptoms.
If not treated, this disease becomes fatal within one
or two years after its symptomatology appears3.
The etiological agents of VL are protozoa of the
Trypanosomatidae family, Leishmania genus; three
species of which may cause the disease: Leishmania
(Leishmania) donovani in Asia and Africa; Leishmania
(L.) infantum in Asia, Europe, and Africa; and
Leishmania (L.) infantum chagasi in the Americas4.
The vectors transmitting the disease are
phlebotomine sand flies (Diptera: Psychodidae:
Phlebotominae); and two species are considered
as vectors in Brazil: Lutzomyia longipalpis (Lutz &
Neivai, 1912) and Lutzomyia cruzi (Mangabeira,
1938), especially the former5.
Dogs (Canis familiaris) are identified as the
main domestic VL reservoir; thus, the detection of
infected animals is crucial in VL control. Even when
they do not display any clinical symptom of the
disease, the animals may act as a source of parasite
infection for phlebotomine sand flies6.
Among the countries in the Americas, Brazil
presents the greatest VL endemicity. The disease
occurs in all five Brazilian regions, with outbreaks
in medium-sized and large urban centers5. Once
considered predominantly rural, VL has undergone
an urbanization process associated with changes in
the behavior of the transmitting vector, environmental
degradation, and the migration of human and
canine populations to larger urban centers 7,8.
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Prado PF et al - Human and canine visceral leishmaniasis in Montes Claros
The strategies recommended by the National Visceral
Leishmaniasis Control Program of Brazil are based on a set of
measures, such as precocious diagnosis and treatment of human
cases, canine serological investigation and culling of all seropositive
dogs, systematic insecticide spraying in domiciles and peridomiciles,
community education programs, and environmental management9.
These measures must be taken together to be effective in reducing
the incidence of the disease.
Incorporating new VL control methodologies in endemic and nonendemic municipalities constitutes a new approach to the problem,
which may help to determine more specific and direct control measures
for each one. Knowing the specific epidemiological features of an area
is crucial in making distinct and adequate measures for each different
situation9. The technological progress achieved since the 1990s has
made it possible to develop and use new tools for describing health
conditions, such as maps that allow observing the spatial distribution
and risk areas. One such tool is geoprocessing, which incorporates
several other technologies for geographical data treatment and
handling10. Geoprocessing has been used in VL planning and control
actions10-14. Data are collected, treated, handled, and presented as
spatial data by means of geographic information systems (SIG)15,16.
VL is endemic in the municipality of Montes Claros, State of
Minas Gerais, where the disease constitutes a serious public health
problem. There are a number of human cases of VL, and both
the population density of the transmitting vector and the canine
prevalence are high17. The aim of this paper is to describe the
epidemiological features of human and canine VL in Montes Claros
from 2007 to 2009 in terms of the vigilance surveillance and control
actions that were implemented in the period.
METHODS
Area of study
Montes Claros (16º43’41’’S, 43º51’54’’W) is located in the
Northern region of the State of Minas Gerais at an altitude of 638m.
The municipality extends over an area of 4,135km2 and has 363,227
inhabitants18. It has a semi-humid tropical climate with a prolonged
dry season.
Georeferenced data
The map of Montes Claros was provided by the City Hall in DWG
file format (AutoCAD program) and converted into Shapefile (shp)
using the Trackmaker and TerraView version 3.14 computer programs.
The addresses of human and canine cases were georeferenced by means
of Garmin GPSMAP 60CSx. The final map was prepared by combining
the data using ArcGIS 3.2 and Mapinfo 7.5. The kernel map for
distributing the density of canine cases was used in the Mapinfo program.
For 2009, four reported cases were not georeferenced: one had
an address that could not be found, one was considered an imported
case by the epidemiological surveillance agents, and two were from
rural areas. Besides, when two or more cases shared the same address,
they were georeferenced as a single point.
RESULTS
For the whole period under study, 95 VL human cases were
reported in the municipality of Montes Claros, for an average of 32.3
cases per year. A total of six deaths were reported: four in 2007, which
revealed an increased lethality coefficient in the series, followed by
one death each in 2008 and 2009 (Table 1). More males were affected
(64%) in the whole period of study. As for the age groups, the 0-9-yearold group was the most affected (48.4%), followed by those 20-39
(20%), 40-59 (15.8%), 10-19 (9.5%), and >60 (6.3%) years old.
As for the canine serological investigation, 46,337 samples were
collected, of which 2,919 (6.3%) were VL-reactive. Table 2 shows
the annual canine samples analyzed, including the seropositivity
prevalence in the series and the amount of euthanized dogs.
Figure 1 shows the human and canine cases in the study period,
allowing certification of the large-scale distribution and overlapping
of both occurrences. It is worth noting that canine seropositivity
coexisted with human disease in all local areas. By visualizing the
risk areas for VL within that municipality as registered in the kernel
map, it can be noted that the areas showing a higher concentration
of cases were localized in the central, northwestern, and southern
regions of the urban area of Montes Claros.
TABLE 1 - Descriptive data of human VL cases in the urban area of Montes Claros,
State of Minas Gerais, Brazil, between 2007 and 2009.
Estimated
Human cases
Confirmed cases of human VL from 2007 to 2009 were analyzed
and registered at the Information System for Disease Notification
(SINAN)19, which is made available by the epidemiological vigilance
service of the Municipal Health Department.
The incidence coefficients and VL lethality per 100,000 inhabitants
were estimated based on the records of confirmed disease cases
and deaths; the population estimates for each year were provided
by the Brazilian Geography and Statistics Institute (IBGE) 18.
Canine cases
Data on serologically reactive dogs for VL in the period of April
2007 to May 2009, as well as the amount of euthanized animals and
the number of implemented actions on VL vigilance and control
were supplied by the local Centro de Controle de Zoonoses (CCZ).
The ELISA (enzyme-linked immunosorbent assay) was the selection
test used in the canine survey, which was later confirmed by indirect
immunofluorescence reaction (IFR), as recommended by the
Brazilian Ministry of Health9.
562
human
VL occurrences (n)
Coefficients
Year
population
cases
deaths
incidence*
lethality (%)
2007
352,384
27
4
7.6
14.8
2008
358,271
35
1
9.7
2.8
2009
363,227
33
1
9.0
3.0
Total
-
95
6
-
-
*per 100,000 inhabitants, VL: visceral leishmaniasis.
TABLE 2 - Canine serological survey for VL in Montes Claros, State of Minas Gerais, Brazil,
between 2007 and 2009.
Dogs
Year
examined
Reactive
2007
14,485
1,041
937
2008
23,884
1,411
1,186
84.0
5.9
2009
7,968
467
358
76.6
5.8
Total
46,337
2,919
VL: visceral leishmaniasis.
Euthanized (%)
90.0
2,481
Prevalence (%)
7.1
-
Rev Soc Bras Med Trop 44(5):561-566, set-out, 2011
N
W
E
S
Human cases of visceral leishmaniasis - 2007
Human cases of visceral leishmaniasis - 2008
Human cases of visceral leishmaniasis - 2009
District of Montes Claros
Urban Area of Montes Claros
Canine cases of visceral leishmaniasis 2007-2009
High density
Low density
3,000
0
3,000
3,000 Miles
Source: Prefeitura Municipal de Montes Claros
FIGURE 1 - Kernel map for canine cases of visceral leishmaniasis in Montes Claros (State of Minas Gerais, Brazil) from 2007 to 2009. The number of human cases
of visceral leishmaniasis per year in the period studied is also indicated.
DISCUSSION
Montes Claros is one of the Brazilian municipalities where VL has
been converted into an urban endemic disease. It has been classified
as an intensive transmission area, in accordance with the stratification
proposed by the Brazilian Ministry of Health9. Its characteristic
urban environment is propitious to VL occurrence, with a climate
and topography favorable for vector proliferation, in addition to the
existence of many extremely poor dwellings lacking basic water and
sewage facilities. In some areas, accumulated organic matter17 becomes
a significant risk factor for the disease. The VL incidence and lethality
coefficients registered in Montes Claros have been above the national
average in recent years, with the former reaching 1.9 cases per 100,000
inhabitants and the latter representing 5.5% of all deaths5. In 2003 and
2004, the municipality faced an epidemic surge with 44 and 68 cases
of human cases of VL, respectively. These numbers corresponded
to incidences of 13.5 and 20.6 cases per 100,000 inhabitants,
accounting for 9.1% and 4.4% of deaths in the respective years.
The first project designed to intensify VL control actions
in Montes Claros was prepared in 2005 in compliance with the
recommendations of the Ministry of Health. Such actions suggested
measures toward controlling the vector and the canine reservoir,
improving the treatment of human cases, environmental management
actions, and educational activities. At the time, the subdivision of
the urban area into 19 sectors was proposed, in accordance with the
identified epidemiological and sociodemographic parameters. In
that year, the risk stratification analysis showed that there were two
intensive transmission areas (n≥4.4, where n is the average number
of human cases of VL in the last 5 years), five moderate transmission
areas (4.4<n≤2.4), and 12 sporadic transmission areas (n<2.4)9.
A survey of infected animals was carried out using ELISA and
IFR for the canine reservoir control, and seropositive dogs were
euthanized as recommended9.
In order to control the vector population density, alphacipermetrine
insecticide was applied in intradomiciles and peridomiciles localized in
districts of moderate VL transmission as well as in districts of sporadic
transmission but high canine VL prevalence. Every dwelling within
urban blocks with confirmed VL human cases was also included.
The environmental management, recorded in a specific form,
consisted surveying the environmental conditions of dwellings, as
well as the number of residents, size of peridomiciles, vegetation
(if absent, shadowy, or shadowless; accumulated organic matters on
the ground, such as leaves, fruits, trunks, roots, domestic animals’
feces), and number of dogs or other existing domestic animals. The
dweller was advised to take preventive measures to reduce favorable
environment conditions for breeding transmission vectors.
Educational health activities were developed through lectures,
meetings, exhibition stands, and visits to households to give
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Prado PF et al - Human and canine visceral leishmaniasis in Montes Claros
the population information on the disease and the relevance of
environmental management, as well as to assure their involvement
and participation in all control actions.
Two years later, in 2007, the stratification analysis pointed to
13 sectors showing sporadic transmission, six others of moderate
transmission, and none of intensive transmission. In 2008 and 2009,
three moderate transmission sectors, 16 sporadic transmission
sectors, and again, no intensive transmission sectors were revealed.
Notwithstanding a high death rate in 2007 (14.8%), the years 2008
and 2009 showed significantly decreased rates of 2.8% and 3%,
respectively. This fact possibly reflects an increased detection of
occurrences due to updated advice delivered by health professionals,
together with the dissemination of information on the disease to
the population, thus reducing late diagnosis, which is considered
one the factors explaining VL lethality9. Figure 2 shows the annual
stratification profiles of VL endemic areas in Montes Claros since
the first intervention carried out in 2005.
FIGURE 2 - Area stratification of transmission risk for VL in the urban area of
Montes Claros (State of Minas Gerais, Brazil) from 2005 to 2009.
The area stratification followed the Brazilian Ministry of Health criteria9, which take
into account the average number of human cases (n) per year in the last 5 years: intense
(n≥4.4), moderate (4.4<n≤2.4), or sporadic (n<2.4). VL: visceral leishmaniasis.
Another factor associated with VL lethality is the inclusion of
the disease in the list of opportunistic infections that affect groups
with comorbidities and individuals infected with the human
immunodeficiency virus (HIV), a population presenting an emerging
highly serious clinical status for VL3. Several studies have shown
the presence of asymptomatic infections by Leishmania chagasi in
VL endemic areas20, 21. Bearing in mind that a HIV-positive patient
in a VL endemic area has 10-100 times higher risk of contracting
the disease22, the HIV infection would have the effect of demasking
the true incidence of Leishmania infection23. The Leishmania-HIV
coinfection occurred in seven patients out of the 95 cases studied
in the municipality.
In the present study, VL was more frequent in children aged 0-9
years, a similar result to that found in the literature5,24,25, although a
change in this profile has been detected, with an increased number
of cases in young adults26,27. The higher susceptibility of children
is explained by their relative cellular immaturity, aggravated by
the malnutrition usually found in endemic areas and even by
564
higher exposure to the vector in the peridomicile5. Epidemiologically
speaking, this also suggests a precocious proximity of humans to the
disease vector in our environment5, a finding that corroborates the
study of Monteiro et al.17, who observed that L. longipalpis was the
prevalent species in both intradomiciles and peridomiciles during an
entomologic survey in the municipality. Another important factor
observed by these authors was that the population density of L. longipalpis
in the local area might be associated with local climate variables
(accumulated rainfall, average temperature, and relative humidity of air)28.
In this study, more male individuals (64%) were affected by VL,
which is compatible with the average of 61% found in the country.
The reason for this has not been completely clarified, although
factors related to gender behavior, such as men’s clothing and the
duration and time schedule of exposure to the vector, could explain
such finding.
Serologically positive dogs were scattered in the municipality,
confirming the influence of this element in human disease. The
serological investigation was carried out with emphasis on vigilance
and control of canine reservoirs in the moderate transmission
sectors. With regard to the sporadic transmission areas as of 2007, an
investigation was accomplished using a sample form, and the results
pointed to a disease prevalence of more than 5%, confirming the need
for a canine census in all sectors of the urban municipal area. This
action was not possible due to operational problems, such as lack of
diagnosis kits, insufficient blood collection personnel, and delayed
acquisition process for equipment needed to implement the ELISA
technique in the CCZ laboratory. The refusal of many owners to
allow diagnosis and euthanasia of seropositive dogs constituted a
hindrance to eliminating canine reservoirs. This was probably due to
both insufficient knowledge of the disease, which stresses the need
for educational measures, and adherence to canine treatment, which
is forbidden by interministerial regulation29. This might also be the
reason for the smallest percentage of euthanasia observed in 2009.
Vigilance and control of vectors have also presented operational
problems, such as lack of insecticides, lack of transport for supervising
activities, and shortage of trained teams for insecticide spraying.
Additionally, the increased incidence of dengue in the municipality
has led health authorities to give priority to measures designed to
address this disease, to the detriment of the planned activities for
VL control. According to the Ministry of Health9, the recommended
activities for vectorial control are dependent on the epidemiological
and entomological features of each locality, as chemical control
should be planned for the period of vector population increase
in the areas of intensive and moderate transmission. Although
the municipality of Montes Claros does not have a structured
entomology laboratory, a partnership with the Instituto René Rachou,
Fundação Oswaldo Cruz (CPqRR/FIOCRUZ) has made it possible
to establish the VL seasonality for the period 2003 to 200817, 28, and
the data obtained are being used in the ongoing program of activities.
As for the environmental management strategy adopted, it
is worth mentioning that Borges30 observed that the chances of
contracting VL are 2.8 times greater in residences where organic
matter is present because sand flies tend to set up their breeding
places in environments rich in organic matter. The results found by
Barata et al. 7 confirm this finding. Other factors related to
environment conditions cited in the literature as being favorable
for the presence of vectors in the peridomicile are chicken yards,
humidity, garbage, and vegetation. The attraction of chicken yards
derives from their function as shelter and food source for the vector.
Rev Soc Bras Med Trop 44(5):561-566, set-out, 2011
As for the health educational activities, the Ministry of Health9
recommends the effective involvement of multi-professional and
multi-institutional teams in articulated actions. The educational actions
developed in the municipality were carried out by the educational
team of the CCZ, which was composed of health surveillance
and environmental technicians, although subject to the available
financial and material resources. Additionally, this team is entitled
to carry out activities in all control programs for endemic diseases,
zoonoses, and urban plagues in the municipal urban and rural areas.
Despite the various possibilities in using a geographic information
system (GIS), in this study it was used only to describe the spatial
distribution of VL cases to call attention to the need for future
investigations of other variables involved in the VL epidemiological
scenario in Montes Claros. The largely scattered spatial distribution
of the disease in this urban area is, undoubtedly, one of the greatest
local public health challenges to be tackled. Several difficulties can be
verified in implementing control activities in view of the insufficient
human, material, and financial resources now available for carrying
out the needed measures in a thorough and integrated way. However,
an analysis of the historical series of VL stratification in Montes Claros
shows that, even in the face of such constraints, human VL cases
decreased, as reflected in the absence of intensive transmission since
2007 as well as the decreased number of moderate transmission areas.
Despite the fact that integrated actions in the whole municipality
have not yet been implemented, the kernel map obtained is able to
point out those areas with a higher risk of VL transmission where
vigilance and control actions should be given priority.
ACKNOWLEDGMENTS
To the staff of the Centro de Controle de Zoonoses (CCZ) of the
Health Department of Montes Claros for their valuable collaboration;
to Fernanda Cristina de Souza Paz for helping with the map; and to
Dr. Consuelo Latorre Fortes-Dias (Fundação Ezequiel Dias, FUNED)
for text criticisms and suggestions.
CONFLICT OF INTEREST
The authors declare that there is no conflict of interest.
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