Home » Volumes » Volume 44 November/December 2011 » Risk factors for Leishmania chagasi infection in an endemic area in Raposa, State of Maranhão, Brazil

Risk factors for Leishmania chagasi infection in an endemic area in Raposa, State of Maranhão, Brazil

Charlene Barreto PonteI; Natália Coelho SouzaI; Maria Neuza CavalcanteII; Aldina Maria Prado BarralIII; Dorlene Maria Cardoso de AquinoI; Arlene de Jesus Mendes CaldasI

IDepartamento de Enfermagem, Universidade Federal do Maranhão, São Luis, MA IIHospital Dr. Odorico Amaral de Matos, Secretaria Municipal de Saúde São Luis, MA IIILaboratório de Imunopatologia, Centro de Pesquisas Gonçalo Moniz, Salvador, BA

DOI: 10.1590/S0037-86822011005000059


INTRODUCTION: Infection with Leishmania chagasi is the most common clinical presentation for visceral leishmaniaisis in endemic areas. The municipality of Raposa is an endemic area in State of Maranhão, Brazil, and have had registration cases of visceral leishmaniasis disease. For this reason, a cross- sectional study was conducted to evaluate the risk factors for infection with L. chagasi detected by Montenegro skin test.
METHODS: The sample comprised 96% of the inhabitants of the villages of Maresia, Pantoja, and Marisol located in the municipality of Raposa, corresponding to 1,359 subjects. Data were collected using a questionnaire. Univariate and multivariate logistic regression models were applied to evaluate the association between the variables studied and infection of L. chagasi.
RESULTS: The variables associated with infection upon nonadjusted analysis were a straw roof, mud walls, floors of beaten earth, presence of sand flies inside or outside of the dwelling, and bathing outdoors. Adjusted analysis showed that the presence of sand flies inside/outside the dwelling was a risk factor, and age younger than 10 years was a protective factor against asymptomatic infection.
CONCLUSIONS: The results highlight the extent to which precarious living conditions of the population strengthen the epidemiological chain of visceral leishmaniasis.

Keywords: Visceral leishmaniasis. Kalazar. Leishmania chagasi. Montenegro skin test. Risk factors.


INTRODUÇÃO: A infecção por Leishmania chagasi é a apresentação clínica mais comum de laishmaniose visceral em áreas endêmicas. O município de Raposa é área endêmica no Estado do Maranhão, tendo registrado casos da doença. Por isso, realizou-se um estudo transversal, com o objetivo de estudar os fatores de risco para infecção por L. chagasi detectada pelo teste intradérmico de Montenegro.
MÉTODOS: O estudo envolveu 96% dos moradores das localidades de Maresia, Pantoja e Marisol do município da Raposa, totalizando 1.359 indivíduos. O levantamento dos dados foi realizado utilizando um questionário. Para verificar a associação entre as variáveis estudadas e a infecção por L. chagasi, foram utilizados os modelos de regressão logística uni e multivariada.
RESULTADOS: Na análise não ajustada, as variáveis associadas à infecção foram: cobertura da casa de palha, paredes de taipa, piso de chão batido, a presença de flebotomíneos dentro ou fora do domicílio e o local do banho fora de casa. Na análise ajustada, a presença de flebotomíneos dentro ou fora do domicílio foi considerada fator de risco e a idade menor que 10 anos revelou-se como fator de proteção para a infecção assintomática.
CONCLUSÕES: Evidenciou-se também, o quanto a precariedade das condições de vida da população contribui para o fortalecimento da cadeia epidemiológica da doença.

Palavras-chaves: Leishmaniose visceral. Calazar. Leishmania chagasi. Intradermorreação de Montenegro. Fatores de risco.




Visceral leishmaniasis is a disease of great concern for public health because of its high incidence and lethality, especially among untreated patients and malnourished children. Visceral leishmaniasis shows a wide geographical distribution and is found in Asia, Europe, the Middle East, Africa, and the Americas. In the Americas, the disease is also called american visceral leishmaniasis (AVL) or neotropical kala-azar1,2.

In Latin America, AVL has been described in at least 12 countries, with 90% of cases occurring in Brazil. The disease is found in 20 states, affecting four of the five regions of the country. The highest incidence is observed in the northeast, accounting for approximately 45% of all cases, followed by the Southeast, North, and mid-west regions1,3,4. The annual average number of cases in Brazil is 3,500. The incidence rate of the disease has reached 20.4 cases/100,000 inhabitants in some places of the Northeastern States such as Piauí, Maranhão, and Bahia. According to official reports, mortality rates can reach 10% in some places1,5.

A spread of AVL to periurban and urban areas has been observed over recent decades. Factors that contributed to the expansion of the disease include transformation of the environment through deforestation and the migration of man from rural areas to the periphery of towns where he lives under precarious conditions of housing and sanitation1, 6, 7.

In Latin America, Leishmania chagasi is the species that is most commonly isolated from patients with AVL8, 9. The most important reservoirs of the parasite in Brazil are dogs and foxes. Transmission occurs indirectly through the bite of the hematophagous sand fly, Lutzomyia longipalpis, whose habitat is the domestic and peridomestic environment where the female feeds on the blood of dogs, humans, other mammals, and birds4, 10-12. Infection with L. chagasi is characterized by a broad spectrum of clinical manifestations ranging from the asymptomatic form to discrete (oligosymptomatic), moderate, and severe manifestations that, if not treated, can lead to the death of the patient12,13. Inapparent or asymptomatic infection is defined as the presence of infection in the absence of clinical manifestations and commonly occurs in patients from endemic areas with epidemiological and immunological evidence of infection14, 15. According to Caldas et al.14, epidemiological surveys conducted in AVL-endemic areas have shown that a portion of the subjects present evidence of infection with L. chagasi in the absence of a history of clinical manifestations, with the observation of high rates of individuals with positive serology (28%) or a positive Montenegro skin test (MST) (19%). Of these, about 20% show clinical manifestations and develop the classical form of the disease, and the remaining ones progress to the oligosymptomatic form or cure1,16.

In Brazil, some individual infections developed by AVL have been observed, and higher rates of infection are monitored in some States such as Bahia (18:1)17, Ceará (11:1)18, and Maranhão (28:1)14. This rate was 5:1 in a study conducted in Kenya2. Therefore, the objective of the present study was to investigate the risk factors for asymptomatic infection with L. chagasi in a population from an AVL-endemic urban area.



A cross-sectional study was conducted between August 2006 and August 2007 in the municipality of Raposa located in the Ilha de São Luis, Northern region of the State of Maranhão. The municipality is organized into towns and villages, the most important being Alto do Farol, Araçagi, Curupu, Vila Pirâmide, Vila Nova, Bom Viver, Maresia, Pantoja, and Marisol12, 19. The present study was conducted in the last three villages.

Maresia, Pantoja, and Marisol are the result of an invasion that occurred approximately 4 years earlier. The economic activity of the residents is based on fishing and handicraft production14. The epidemiology of AVL in these villages was responsible for 20% of the AVL cases registered in the municipality in 2003 and 34% in 200412. This place was chosen for the study because it is a recent endemic area of AVL20.

The sample comprised 96% of the residents of Maresia, Pantoja, and Marisol who met the following inclusion criteria: living in one of the three villages for more than 6 months and no past or present history of AVL.

The study was designed and conducted in two phases: In the first phase, a population census was performed; in the second phase, a questionnaire was used for the collection of demographic, socioeconomic, and epidemiological data. In addition to the use of questionnaire, the subjects were submitted to physical examination and the Montenegro skin reaction for the detection of infection with Leishmania sp. The antigen was prepared by the Gonçalo Moniz Research Center/FIOCRUZ, Salvador, BA, from promastigote forms of L. amazonensis (MHOMBr-88-BA-125). An induration diameter of >5mm was defined as a positive reaction.

The data were analyzed with the Epi-Info 3.3.2 program of the World Health Organization. The variables were classified into two or more categories, with the first being considered the baseline category the one associated with the lowest risk. For analysis of the ass/ociation between the variables studied and infection with L. chagasi, the relative risk (RR) and its respective 95% confidence interval adjusted or not for the prevalence of infection detected by the MST were calculated. Adjusted analysis, including all variables that presented a p value <0.20, was performed by logistic regression using the STATA 9.0 program.

Ethical considerations

The study was approved by the Ethics Committee of the University Hospital, Federal University of Maranhão (protocol 33104-444/2006). The wish and decision of the participant or responsible person were respected throughout the study. All subjects signed a free informed consent form.



The census performed in the villages of Maresia, Pantoja, and Marisol, municipality of Raposa, MA, revealed a population of 1,417 inhabitants; of these, 1,359 fulfilled the inclusion criteria and accepted the request to be part of the study population. Analysis of the demographic data showed that the age group of 0 to 10 years was associated with L. chagasi infection, which was a protective factor for infection (Table 1). For the type of housing, the variables associated with infection were a straw roof (RR=1.06, p=0.0412), mud wall (RR=1.08, p=0.007), straw wall (RR=1.11, p=0.040), and floor of beaten earth (RR=1.07, p=0.007) (Table 1). Household income (0.0562) and disposal of garbage (0.0512) in the open air showed a borderline significant p value, indicating a possible association with L. chagasi infection (Table 1).



Regarding the other variables, insecticide spraying, presence of animals in the domestic or peridomestic area and life habits, the presence of a pig pen close to the dwelling, presence of sand flies, and bathing outdoors (backyard) were associated with L.chagasi infection (Table 2).



Variables that continued to be associated with infection upon the adjusted analysis were age of 0-10 years as a protective factor and the presence of sand flies inside and outside the dwelling (Table 3).




Visceral leishmaniasis is endemic in Ilha de São Luis since the 1980s5, and an increased rate of migration of individuals from rural to urban areas and from other states has been observed during this period. These people settled in overcrowded and inadequate settlements constructed at the periphery of Ilha de São Luis (consisting of four municipalities), generally in recently inhabited and occupied areas characterized by deforestation and burning21, 22. These conditions offer an excellent habitat for Lu. Longipalpis, and the density of this species can reach elevated levels inside dwellings and animal shelters. This sociogeographic profile applies to many of the residents of Marisol, Pantoja, and Maresia.

In the present study, the proportion of infection detected by the MST was more frequent among individuals older than 10 years. A higher incidence of infection in the population older than 10 years was also reported by Moreno et al23. About 30% of adults from endemic areas without a history of the disease present a strong positive skin test. This finding might be explained by a longer time of exposure to the parasite, conferring higher resistance against the disease; a positive MST indicates that one individual is not sick and that his cellular immunity is satisfactory at that time23,24.

Studies have demonstrated differences in the age group affected between asymptomatic Lchagasiinfection and AVL disease, with the observation of a lower proportion of asymptomatic infection in children younger than 10 years. However, this age group is more affected by the disease14, 18. The higher susceptibility of children of this age to the clinical form of the disease is probably due to higher rates of nutritional deficiencies and consequent lower immunological resistance5,18,24.

Roof, wall, and floor materials of the dwelling were risk factors for infection with L. chagasi. The type of housing, with mud construction and straw roofs, facilitates the entry of the vector through holes and other openings4, 21. Borges25 observed that plastered walls offer more protection for residents against AVL than a non-plastered dwelling.

Nascimento et al.5 showed that environments of low socioeconomic level are prone to the occurrence of AVL, affecting human settlements characterized by precarious housing conditions. In the study of Silva et al.7 including patients from Ilha de São Luis with a diagnosis of visceral leishmaniasis, the dwellings visited were mainly made of mud (68%) and had a straw roof (48%) and floor of beaten earth (66%), which were in agreement with the present findings.

The variable, household income, showed borderline significance (p=0.0562), with a substantial number of subjects infected with L. chagasi earning less than two minimum wages (92%). This result agrees with the findings of Caldas et al.21 who also studied a sample from the municipality of Raposa, MA, and observed that most children were from families earning less than two minimum wages. The mean monthly household income was 1.7 minimum wages (U$315,112), demonstrating the conditions of poverty of this population.

The destination of household waste is an important variable for the epidemiology of AVL, as household waste serves as a potential breeding site for the vectors. This was demonstrated by Borges25 who observed an increase in the chance of contracting visceral leishmaniasis among residents of areas where no system of garbage collection is available. In the present study, waste destination also showed borderline significance (p=0.0512) similar to the type of housing.

Although the dog is an important element in the epidemiological chain of AVL, no significant association was observed between the presence of dogs in domestic or peridomestic areas and infection with L. chagasi. Nascimento et al.5 and Caldas et al.21 also found no association between the presence of dogs in domestic/peridomestic areas and L. chagasi infection; thus, this variable was not considered a risk factor.

The presence of sand flies inside and outside the dwelling was a risk factor for infection with L. chagasi. Similar results were reported by Caldas et al.21 who studied L. chagasi infection in children from the same municipality and observed that the chance of infection was almost two times higher among children living in houses with sand flies compared to those living in houses without these insects. Another risk factor was bathing outdoors. Generally, people take a bath outdoors.

Lu. longipalpis easily adapts to the peridomestic area and variable temperatures and can be found inside dwellings and in shelters of domestic animals1. According to Rebelo et al.26, the rapid adaptation of this vector to peridomestic environments in rural areas and even in peripheral neighborhoods of large urban center is due to the progressive modification of the primitive vegetation at these sites.

According to Cebino Neto27, the neighborhoods with predominant vegetation covering that passed through a messy occupation, followed by an increase population density, have registered the highest incidence rates of visceral leishmaniasis. Trees and plantations around the houses have been treated as a significant factor of Kala azar. According to Ranjan et al28, some trees are considered source of fructose for Phlebotomine sandflies and also produce dark and damp environments around the peripheral neighborhood, the ideal places of shelter for the mosquito.

Knowledge about the risk factors for infection with L. chagasi is the first step to the elaboration of more effective control strategies. Collective health measures designed to improve the overall living conditions of this population need to be implemented.



We thank the Municipal Secretariat of Health of Raposa, Maranhão for the participation of its community health agents in the active identification of the subjects for the study. We are also indebted to the communities of the villages of Maresia, Pantoja, and Marisol that, in a gesture of selflessness, agreed to participate in the study.



Fundação de Amparo a Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).



1. Ministério da Saúde. Manual de controle da leishmaniose visceral. Brasília: Ministério da Saúde; 2008.         [ Links ]

2. World Health Organization. Control of leishmaniasis. Geneva: World Health Organization; 1990.         [ Links ]

3. Moreira JRED, Torre EB, Lobo CFL. Urbanização do calazar ou ruralização da periferia dos centros urbanos? Rev Soc Bras Med Trop 2006; 33:100.         [ Links ]

4. Werneck GL. Forum: geographic spread and urbanization of visceral leishmaniasis in Brazil. Cad Saude Publica 2008; 24:2937-2940.         [ Links ]

5. Nascimento MDSB, Souza EC, Silva LM, Leal PC, Cantanhede KL, Bezerra GFB, et al. Prevalência de infecção por Leishmania chagasi utilizando os métodos de ELISA (rK39 e CRUDE) e intradermorreação de Montenegro em área endêmica do Maranhão, Brasil. Cad Saude Publica 2005; 21:1801-1807.         [ Links ]

6. Rosas-Filho MS, Silveira FT. Epidemiologia, clínica e imunologia da infecção humana por Leishmania (Leishmania) infantum chagasi em área endêmica de Leishmaniose Visceral no Pará. Rev Paraense Med 2007; 21:7-18.         [ Links ]

7. Silva AR, Tauil PL, Cavalcante MNS, Medeiros MN, Pires BN, Gonçalves EGR. Situação epidemiológica da leishmaniose visceral, na ilha de São Luís, Estado do Maranhão. Rev Soc Bras Med Trop 2008; 41:358-364.         [ Links ]

8. Moreno EC, Melo MN, Genaro O, Lambertucci JR, Serufo JC, Andrade ASR, et al. Risk factors for Leishmania chagasi infection in an urban area of Minas Gerais State. Rev Soc Bras Med Trop 2005; 38:456-463.         [ Links ]

9. Queiroz MJA, Alves JGB, Correia JB. Visceral leishmaniasis: clinical and epidemiological features of children in an endemic area, Porto Alegre. Journal Ped 2004; 80:142-146.         [ Links ]

10. Aguiar Z, Ribeiro MCS. Vigilância e Controle das Doenças Transmissíveis. 2nd ed. São Paulo: Martinari; 2006.         [ Links ]

11. Gontijo CMF, Melo MN. Leishmaniose visceral no Brasil: quadro atual, desafios e perspectivas. Rev Bras Epi 2004; 7:338-349.         [ Links ]

12. Fundação Nacional de Saúde. Resumo do Sistema de Reconhecimento Geográfico do Município da Raposa-MA. Ministério da Saúde; 2005.         [ Links ]

13. Marzochi MCA, Sabroza PC, Toledo LM, Marzochi KB, Tramontano NC, Rangel-Filho FB. Leishmaniose visceral na cidade do Rio de Janeiro, Brasil. Cad Saude Publica 1985; 1:5-17.         [ Links ]

14. Caldas AJM, Silva DRC, Pereira CCR, Nunes PMS, Silva BP, Silva AAM, et al. Infecção por Leishmania (Leishmania) chagasi em crianças de uma área endêmica de leishmaniose visceral americana na Ilha de São Luis-MA, Brasil. Rev Soc Bras Med Trop 2001; 34:445-451.         [ Links ]

15. Gama MEA, Costa JML, Gomes CMC, Corbett CEP. Subclinical form of the American Visceral Leishmaniasis. Mem Inst Oswaldo Cruz 2004; 99:889-893.         [ Links ]

16. Jeronimo SMB, Teixeira MJ, Sousa AQ, Thielking P, Pearson RD, Evans TG. Natural history ofLeishmania (Leishmania) chagasi infection in Northeastern Brazil: Long-term follow-up. Clinical Infec Dis 2000; 30:608-609.         [ Links ]

17. Badaró R, Jones TC, Carvalho EM, Pedral-Sampaio D, Reed SG, Barral A, et al. New perspectives on a subclinical formo f visceral leishmaniasis. J Inf Dis 1986; 154:1003-1011.         [ Links ]

18. Evans TG, Vasconcelos IAB, Lima JW, Teixeira JM, McAullife IT, Lopes UG, et al. Epidemiology of visceral leishmaniasis in northeast Brazil. Journal Infec Dis 1992; 166:1124-1132.         [ Links ]

19. Instituto Brasileiro de Geografia e Estatística. Tendências demográficas: uma análise da população com base nos resultados dos censos demográficos de 1940 e 2000 [Internet]. Brasília: IBGE. 2007 – [cited 2009 January 15]. Available from: http://ibge.gov.br/home/presidencia/noticias_visualiza.php?id-noticia=892&idpagina=1/.         [ Links ]

20. Ministério da Saúde. Sistema de Informação de Agravos de Notificação. Brasília: Ministério da Saúde. 2007 – [cited 2009 March 22]. Available from: http://dtr2004.saude.gov.br/sinanweb/novo/.         [ Links ]

21. Caldas AJM, Costa JML, Silva AAM, Vianhais V, Barral A. Risk factors associated with asymptomatic infection by Leishmania chagasi in northeast Brazil. Trans R Soc Trop Med Hyg 2002; 95:1-8.         [ Links ]

22. Costa JM, Viana G, Saldanha A, Nascimento M, Alvim A, Burattini M, et al. Leishmaniose visceral no estado do Maranhão, Brasil: a evolução de uma epidemia. Cad Saude Publica 1995; 11:321-324.         [ Links ]

23. Moreno EC, Melo MN, Genaro O, Lambertucci JR, Serufo JC, Andrade ASR, et al. Risck factors for Leishmania chagasi infection in a urban área of Minas Gerais State. Rev Soc Met Trop 2005; 38:456-463.         [ Links ]

24. Crescente JAB, Silveira FT, Lainson R, Gomes CMV, Laurenti MD, Corbett CEP. A cross-sectional study on the clinical and immunological spectrum of human Leishmania (L.) infantum chagasiinfection in the Brazilian Amazon region. Trans Soc Trop Med Hyg 2009: 103:1250-1256.         [ Links ]

25. Borges BKA. Fatores de risco para leishmaniose visceral em Belo Horizonte [Masther´s disssertation]. [Belo Horizonte (MG)]: Universidade Federal de Minas Gerais; 2006.         [ Links ]

26. Rebêlo JMM, Araújo JC, Carvalho ML. Flebótomos (Lutzomyia, Phlebotominae) da Ilha de São Luís, zona do Golfão Maranhense, Brasil. Rev Soc Bras Med Trop 1999; 32:247-253.         [ Links ]

27. Cerbino-Neto J, Werneck GL, Costa CHN. Factors associated with the incidence of urban visceral leishmaniasis: an ecological study in Teresina, Piauí State, Brazil. Cad Saude Publica 2009; 25:1543-1551.         [ Links ]

28. Ranjan A, Sur D, Singh VP, Siddique NA, Manna B, Lal CS, et al. Risk factors for Indian kala-azar. Am J Trop Med Hyg 2005; 73:74-78.         [ Links ]



 Address to:
Dra. Arlene de Jesus Mendes Caldas
Depto. Enfermagem/UFMA
Rua Viana Vaz 230, Centro
65020-660 São Luis, MA, Brasil
Phone: 55 98 3301-9701; 3227-8519; 9971-2421
e-mail: ajmc@elo.com.br

Received in 23/11/2010
Accepted in 05/05/2011