• 1

    World Health Organization, Leishmaniasis. Geneva, WHO. Available at: http://www.who.Int/leishmaniasis. Accessed August 10, 2007.

  • 2

    Brasil, Ministério da Saúde, Secretaria de Vigilância à Saúde, 2007. Manual de Vigilância da Leishmaniose Tegumentar Americana. Second edition. Brasília, DF.

  • 3

    Alacais A, Abel L, David C, Torrez ME, Flandre P, Dedet JP, 1997. Risk factors for onset of cutaneous and mucocutaneous leishmaniasis in Bolivia. Am J Trop Med Hyg 57 :79–84.

    • Search Google Scholar
    • Export Citation
  • 4

    Davies CR, Llanos-Cuentas EA, Campos P, Mange J, Villaseca P, Dye C, 1997. Cutaneous leishmaniasis in the Peruvian Andes: risk factors identified from a village cohort study. Am J Trop Med Hyg 56 :85–95.

    • Search Google Scholar
    • Export Citation
  • 5

    Chaves LF, Cohen JM, Pascual M, Wilson ML, 2008. Social exclusion modifies climate and deforestation impacts on a vector-borne disease. PLoS Negl Trop Dis 2 :e176.

    • Search Google Scholar
    • Export Citation
  • 6

    Ampuero J, Urdaneta M, Macêdo VO, 2005. Factores de riesgo para la transmission de leishmaniasis cutánea em niños de 0 a 5 años en un área endémica de Leishmania (Viannia) brasiliensis. Cad Saude Publica 21 :161–170.

    • Search Google Scholar
    • Export Citation
  • 7

    Sosa-Estani S, Segura EL, Gómez A, Salomón OD, Peralta M, Coutada V, Ruiz LM, 2001. Leishmaniose cutânea no Norte da Argentina. Fatores de risco identificados num estudo caso-coorte em três municípios de Salta. Rev Soc Bras Med Trop 34 :511–517.

    • Search Google Scholar
    • Export Citation
  • 8

    Yadon ZE, Rodrigues LC, Davies CR, Quigley MA, 2003. Indoor and peridomestic transmission of American cutaneous leishmaniasis in northwestern Argentina: a retrospective case-control study. Am J Med Hyg 68 :519–526.

    • Search Google Scholar
    • Export Citation
  • 9

    Instituto Arnon de Melo, 2006. Enciclopédia Municípios de Alagoas. Maceió, AL.

  • 10

    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.

    • Search Google Scholar
    • Export Citation
  • 11

    Lins ALGO, 1996. Leishmaniose tegumentar de americana—estudo epidemiológico em Pernambuco no período 1985–1994. Master dissertation. Recife-PE: Universidade Federal de Pernambuco.

  • 12

    Aguiar GM, Medeiros WM, 2003. Distribuição e habitat. Rangel EF, Lainson R, eds. Flebotomíneos de Brasil. Fiocruz, 207–256.

  • 13

    Bern C, Hightower AW, Chowdhury R, Ali M, Amann J, Wagatsuma Y, Haque R, Kurkjian K, Vaz LE, Begum M, Akter T, Cetre-Sossah CB, Ahluwalia IB, Dotson E, Secor WE, Breiman RF, Maguire JH, 2005. Risk factors for kala-azar in Bangladesh. Emerging Infectious Diseases. Volume 11. Available at: www.cdc.gov/eid. Accessed September 15, 2007.

  • 14

    Afonso MMS, Gomes AC, Meneses CRV, Rangel EF, 2005. Studies on the feeding habits of Lutzomyia (N) intermedia (Diptera, Psychodidae), vector of cutaneous leishmaniasis in Brazil. Cad Saude Publica 21 :1816–1820.

    • Search Google Scholar
    • Export Citation
  • 15

    Marassá AM, Consales CA, Galati EAB, Nunes VLB, 2006. Identificação do sangue ingerido por Lutzomyia (Lutzomyia) longipalpis (Lutz & Neiva, 1912) e Lutzomyia (Lutzomyia) almeriori (Galati & Nunes, 1999) pela técnica imunoenzimática do ELISA de captura, no sistema avina-biotina. Rev Soc Bras Med Trop 29 :183–186.

    • Search Google Scholar
    • Export Citation
  • 16

    Reithinger R, Davies CR, 1999. Is the domestic dog (Canis familiaris) a reservoir host of American cutaneous leishmaniasis? A critical review of the current evidence. Am J Med Hyg 61 :530–541.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 
 
 

 

 

 

 

 

 

Sociodemographic and Environmental Risk Factors for American Cutaneous Leishmaniasis (ACL) in the State of Alagoas, Brazil

View More View Less
  • 1 Instituto de Ciências Biológicas e da Saúde (ICBS), Universidade Federal de Alagoas (UFAL), Prado, Maceió-AL, Brasil; Departmento de Medicina Tropical, Centro de Ciências da Saúde (CCS), Hospital das Clínicas, Universidade Federal de Pernambuco (UFPE), Cidade Universitária, Recife-PE, Brasil

The multiplicity of factors involved in the transmission of the American cutaneous leishmaniasis (ACL) constitutes a challenge to its control. Thus, knowledge of such factors may contribute extremely toward redefining the control strategies. The aim of this study was to identify sociodemographic and environmental factors relating to ACL transmission in the State of Alagoas, Brazil. A case-control study with incident cases was conducted. Diagnostic criteria were the presence of compatible skin lesions, laboratory confirmation, and clinical cure after treatment. Two control groups were matched to cases by sex and age: one comprising neighbors and the other from a community-based draw; controls were individuals with no lesion and a negative Montenegro intradermal reaction. Between July 1, 2004 and February 1, 2007, 98 cases and the same number of controls per group were selected. In the multivariate analysis, for both control groups, ACL was associated with absence of a gas stove and forest less than 200 m away; for neighborhood controls with schooling of 4 years or less, family income greater than one minimum salary, birds inside the home, forest-related leisure activities, and rural work or school activities; and for community controls with non-durable wall material in the house, per capita income greater than US$ 28.31, animals inside the house, and absence of dogs and cats around the house. Specific control measures are recommended for areas with similar characteristics: protection for individuals undertaking forest-related leisure activities; distancing houses from forests by more than 200 m; and elimination of bird or other animal-rearing inside homes. General measures of improved housing and living conditions are also recommended.

INTRODUCTION

According to the World Health Organization (WHO), it is estimated that 350 million people around the world in 88 countries live in places with the risk of contracting leishmaniasis.1 In Brazil, the number of detected cases of American cutaneous leishmaniasis (ACL) has remained stable, ranging from 30,873 in 2003 to 23,892 in 2006.2 In the State of Alagoas, there has been a similar pattern, with some variation year by year: 87 cases in 2002, 97 cases in 2003, 63 cases in 2004, 56 cases in 2005, and 43 cases in 2006.

One of the great difficulties in undertaking control measures against ACL has been the multiplicity of factors involved in its transmission. The diversity of etiologic agents, variety of vector species, existence of both wild and domestic reservoirs, differences in environmental conditions (involving climate, vegetation, rainfall, and altitude), and differences in human factors (such as individual habits, housing conditions, work conditions, and leisure activities) could all play a role either in transmission or in the outcome of the infection.2 Some studies focus on some specific topics aiming to identify and measure risks related to migratory characteristics3 or vector prevalence,4 deforestation5 or solely investigated children.6 There are few analytical studies on ACL with a wider approach. 7,8

Knowledge of risk factors for a disease that are identified from analytical epidemiologic studies may contribute toward the implementation of protection measures, thereby reducing the impact of the disease on the community. Specifically in the case of ACL, knowledge of such factors may contribute extremely toward redefining the control strategies. The aim of this study was to identify sociodemographic and environmental factors relating to ACL transmission in the State of Alagoas.

METHODOLOGY

Study area.

The State of Alagoas is located in the central-eastern portion of the northeastern region of Brazil. It has an area of 27,767.6 km2 (Figure 1) and 2,822,621 inhabitants (2007). The altitude is generally less than 300 m and the climate is typically humid tropical, with a mean annual temperature of 25°C and mean annual rainfall of 1410 mm.9

In the State of Alagoas, American cutaneous leishmaniasis occurs more frequently in the East Mesoregion, mainly near the border with the state of Pernambuco. Males, adults, and residents of rural areas are those more often affected.2 Cutaneous single lesions are more prevalent, Leishmania (Viannia) brasiliensis being the only agent found.

The pattern of transmission in this state is rural and periurban, differing from that found in the Amazon Region, either in Brazil or other South American countries. In the Amazon it is a zoonosis of wild animal reservoirs whose transmission is related either to the human contact with primary forests, or to the disordered exploitation of forests for extractive activities, construction of roads, agriculture, and cattle raising or, still, to ecologic tourism.

Study design and population.

A case-control study was carried out and the group of cases consisted of incident cases diagnosed between July 1, 2004 and February 1, 2007, among individuals living in the State of Alagoas. The following criteria were used for the diagnosis of cases: 1) presence of skin ulcers with raised rims and granular base, 2) either a positive Montenegro intradermal reaction and/or the finding of the parasite through direct and/or histopathologic examination, 3) therapeutic response and healing of the lesions (Figure 1). Cases with late mucous lesions, human immunodeficiency virus (HIV), and acquired immunodeficiency syndrome (AIDS) coinfection were excluded. The main considerations in the differential diagnosis were bacterial ulcers, vascular ulcers, sporotrichosis, squamous cell carcinoma, and leprosy, which are distinguishable from ACL by the criteria used.

Two independent control groups were formed: one consisting of neighbors of the cases and the other of individuals within the community. Neighborhood controls were selected using a systematic routine, starting from the address of the case. The first house on the left side was visited to identify individuals who would meet the selection criteria. If no one was enrolled, the houses on the same side would be sequentially visited until individuals that would fulfill the requirements for controls were identified and accepted to be part of the study. When there was more than one individual with the same sex and in the same age group as the case, the one with the closer age to the latter would be selected. Neighbors would share the same environment as the cases and, thus, differences in the frequency of the disease would be expected to be related to differences in habits. The latter were selected by means of a draw among families living in the area who were receiving care from the Family Health Program team. If they did not live close to the cases, their comparison with the latter would allow a better understanding of the role of environmental factors . Individuals who had moved into the area less than one year earlier, those with past or present skin and/or mucous lesions compatible with ACL, those with antecedents of ACL, and those with a positive Montenegro intradermal reaction were excluded (all controls were tested). Controls were matched to cases by sex and age. The following upward or downward limits for age-matching were observed: for cases less than 2 years of age, the age difference for controls would not exceed 2 years; for cases between 2 and 4 years of age, the age difference for controls would not exceed 3 years; for cases between 5 and 19 years of age, the age difference for controls would not exceed 5 years; for cases between 20 and 59 years of age, the age difference for controls would not exceed 10 years; and for cases greater than or equal to 60 years of age, the age difference for controls would not exceed 20 years (Figure 2).

The Montenegro skin test consisted of the intradermal application of 0.1 mL of the antigen Leishmania (Leishmania) amazonensis, strain OMS MHOM/BR/73/PH8. The size of induration was measured after 48 to 72 hours and an induration of 5 mm or larger was considered a positive result.

Sample size.

The sample size calculation was based on the following parameters: an alpha error of 5% and a beta error of 20% (corresponding to a power of 80%). For the proportion of the baseline population that is exposed, three variables were considered based on the work of Soza-Estani and others7: staying out of the household for more than 10 hours (27.6%), performing domestic work out of the household (15.4%), and windows that cannot be locked in the closed position (20%), with odds ratios (ORs) of 2.35, 3.69, and 2.63, respectively. The largest sample size obtained was 104 cases and 104 controls for staying out of the household for more than 10 hours.

Data collection.

The data collection was carried out by one of the researchers. Potential cases were reported to the researcher mainly by the municipal epidemiologic surveillance teams and family health teams, which had been previously trained (by the researcher). Cases were also identified by means of data from reference services and from the National Disease Notification System (SINAN). Interviews using the same standardized questionnaire were conducted with cases and both groups of controls. The questionnaire was drawn up to obtain data on the following groups of variables: sociodemographic variables (sex, age, schooling, income, place of origin); variables relating to work, school, or leisure activities (location of the work or school activity, frequenting of transmission areas, time in hours dedicated to the principal professional activity, ecotourism, mean length of time per day spent outside of the house, and sleeping at the workplace); variables relating to activities outside of the house (hunting, fishing, performing domestic activities outdoors, walking in the fields at night or at dusk, gathering firewood, and collecting water); variables relating to domestic habits (sleeping under a mosquito net, sleeping outdoors, combating insects—use of insecticide in the previous 30 days—use of repellents, and sleeping with the window open); variables relating to the household (wall material, roofing material, number of rooms, number of bedrooms, number of people per bedroom, water supply, bathroom, toilet, electricity, gas stove, and location of the house); and variables relating to the area surrounding the household and the environment (forest close to the house, river close to the house, crops close to the house, neighbors’ houses nearby, domestic animals inside the house, and domestic animals outside of the house).

Data analysis.

The data were processed using the Epi Info software (version 6.04, CDC, Atlanta, GA), with double data entry. The analysis was performed using Stata 9.2 (StataCorp, College Station, TX), with conditional logistic regression.

Association between American cutaneous leishmaniasis (ACT) and each potential risk factor was studied. As it was a matched case-control study (matched for sex and age), a matched analysis was performed using conditional logistic regression. Univariate conditional logistic regression was used to obtain matched ORs, 95% confidence intervals (CIs), and a likelihood ratio test P values. Those variables which, in the univariate analysis, showed an association with the outcome with a P value < 0.10 were introduced in the multivariate model. A forward selection technique was performed to obtain a final multivariate model in each block. A variable would remain in the model either if it were significantly associated with the outcome (P < 0.05) or if it changed the value of the OR estimated for other variables by more than 10%.

The research project was approved by the research ethics committee of the Federal University of Alagoas (UFAL), under the procedure number CEP-02/2004.

RESULTS

Ninety-eight cases were selected and 196 controls, in two groups of 98 each, were also selected. Most of the ACL patients were males (64.3%) with a mean and media age of, respectively, 27.4 and 22.5 years. Although most of them were in the age group 20 to 49 years (39.8%), there were an important proportion of cases in younger ages: 15.3% in the age group 1 to 9 years and 30.6% in the age group 10 to 19 years. More than half (58.2%) of the patients had a single lesion, 39.8% had multiple lesions, and 2% had disseminated lesions. Most of them (78.5%) were from rural localities.

In relation to the neighborhood controls, the best multivariate model for sociodemographic variables consisted of more than 4 years of schooling and family income greater than or equal to one minimum salary (Table 1). For the block of variables relating to work, school, or leisure activities together with the variables relating to activities outside of the house, the best multivariate model consisted of rural location for work or school activities and forest-related leisure activities (Table 2). For the variables relating to the household, a statistically significant association was observed only for the presence of a gas stove in the house, and there were no other variables to adjust for in the multivariate model. For the variables relating to the area surrounding the household and the environment, the best model consisted of birds inside the house and forest less than 200 m away (Table 4).

In relation to the community controls, the best adjusted model for sociodemographic variables consisted of more than 4 years of schooling and family per capita income greater than US$ 28.31 (Table 1). For the variables relating to work, school, and leisure activities together with the variables relating to activities outside of the house, the best multivariate model consisted of rural location for work or school activities and the habit of fishing (Table 2). For the variables relating to the household, the best adjusted model consisted of absence of a gas stove in the house and presence of non-durable wall material (Table 3). For variables relating to the area surrounding the household and the environment, the best multivariate model consisted of presence of animals inside the house, forest less than 200 m away, dogs outside of the house, and cats outside of the house (Table 4).

For the neighborhood controls, an analysis was performed with all the variables relating to factors within the house that were associated with ACL transmission, including the sociodemographic variables and those relating to the household. Absence of a gas stove in the house, more than 4 years of schooling, and family income greater than or equal to one minimum salary remained in the model (Table 5). Another adjusted model was constructed using the factors external to the house and, for this, variables relating to work, school and leisure activities, habits outside of the house, the area surrounding the household, and the environment were used in the analysis. This model was adjusted for the presence of birds inside the house, leisure activities in the forest, presence of forest less than 200 m from the house, and rural location for work or school activities (Table 6).

For the community controls, the best adjusted model for sociodemographic variables with those for the household consisted of absence of a gas stove in the home, non-durable wall material in the house, and per capita family income greater than US$ 28.31 (Table 5). Among the variables relating to work, school and leisure activities, activities outside of the house, the area surrounding the household, and the environment, only the variables relating to the area surrounding the household and the environment remained in the model, thus repeating the previous model (Table 6).

DISCUSSION

In this study, two control groups were used. The use of neighborhood controls was aimed at matching with cases according to environmental conditions and making it possible to adequately evaluate associations related to habits. The community controls allowed better assessment of the associations with environmental factors.

One frequent limitation in this type of study is selection bias. If it occurred in this study, it was of small magnitude. One patient, with a diagnosis confirmed by laboratory tests and cure after treatment, refused to participate and it may have happened that four patients were not included (selection failure) because of deficiencies in the laboratory tests used. The presence of the researcher and the whole collaborating team in the municipalities where ACL is endemic led to notification of almost all the cases detected. With regard to information bias, the rigid criteria for identifying cases and controls are expected to have reduced classification errors relating to the outcome to a minimum. Malnutrition or host genetics were not assessed and thus the confounding effect of these variables could not be estimated. Furthermore, some of the factors studied may be a proxy indicator for poverty in our study population, being some of the mediators between ACL and poverty. Finally, the number of regression analyses that were carried out may have increased the chance of an alpha error.

Sociodemographic variables.

It was observed that schooling presented an association with ACL, because individuals with more than 4 years of schooling—reflecting their better social condition—presented a lower chance of becoming diseased. Surprisingly, individuals in the higher category of family income had a greater chance of acquiring ACL. This association remained even after adjusting income for the other factors, and the mechanism for this association is unclear. A possible explanation to this finding would be an information bias. People may have not given accurate information on income, either because they did not want to declare their income or because they may have some difficulty in estimating their earnings. As the sampled population was mainly composed of people living in small towns or rural areas, their earnings often are not regular and some of them grow subsistence crops, which they do not add to their earnings. Thus, family income may not be the factor that best expresses living conditions in this area.

Among this population, which was composed mainly of people living in small towns or in rural areas, family income may not be the factor that best expresses living conditions, unless there was some information bias.

Work, school, or leisure activities.

Rural work or school activity was a risk factor for acquiring ACL. However, no association was observed with the time spent on such activities or with the length of time spent away from the house, as shown in another study.7 Having leisure activities in the forest increased the chance of acquiring ACL by a factor of around six times, when comparison was made with neighborhood controls.

Activities outside the home.

With community controls it was found that the activity of fishing and water collection outside of the house decreased the chance of ACL, contrary to what was expected and what had been reported by other authors, 7,8,10 considering that remaining outside of the house ought to increase the chance that individuals would acquire ACL. Some divergences found between different studies may have resulted from differences between the vector species that are responsible for ACL transmission in each locality. These species may present different habits and thus modify the risk related to these human activities.

In using neighborhood controls, the variables relating to individual activities (rural work or school activities, leisure activities in the forest, and hunting) presented greater strength of association with acquisition of ACL, thus expressing a close association between exposure to the environment outside the house and the chance of transmission. The activities of hunting and undertaking leisure activities in the forest are closely related. Using these two variables in the multivariate analysis, among neighborhood controls, the activity of hunting lost its statistical significance (data not presented), which is a very plausible result, considering that both of these activities have a direct relationship with exposure to the wild environment (forest) and to vector bites.

However, the multivariate analysis on the same groupings of variables among the community controls reinforced the hypothesis that the activity of fishing decreased the chance that the individuals would acquire ACL, since the association was maintained even after adjustment for variables expressing rural work or school activities.

Variables relating to domestic habits.

The absence of any association for variables relating to domestic habits in the two control groups suggests that the risk factors listed were not associated with ACL transmission in Alagoas, and/or that the low frequency of responses for some variables limited the interpretation of these findings.

Absence of a gas stove in the house was shown to be a risk factor for ACL in relation to both control groups. This may be interpreted as another measurement of social condition. This finding may also be related to a possible confounding factor. Individuals who do not have a gas stove probably cook using firewood, a practice that is often carried out outdoors, thus leading to exposure to sandfly bites in the area outside the house. However, the location of the kitchen was not a variable investigated in this study. Cooking using firewood may also be associated with gathering firewood in the countryside, which was a variable with no statistically significant association with ACL.

Variables about home.

The association with non-durable wall material in the house, among community controls, suggests that precarious living conditions increase the chance of acquiring ACL. This finding can be understood as a measurement of social condition or a situation that facilitates access to the house by vectors, through the gaps in the walls.

Variables about the area surrounding the home.

The presence of forest less than 200 m away from the house was a risk factor for both controls, thus reflecting its importance for transmission relating to breeding sites and transmitter dispersion capacity.8

Although the type of crop was not among the variables studied, it could be seen during the data collection that banana cultivation was often present in the ACL transmission areas, and this might be associated with specific breeding sites for the probable vector(s). Data in the literature suggest that the vector species Lutzomyia whitmani, L. intermedia, and L. migonei are the ones that are most common in Alagoas, and these are found associated with banana plantations. 2,11,12

Animal-rearing inside the house was associated with ACL transmission, for both control groups, independent of the animal species. This association remained when the creatures studied were birds, with increasing risk as the number of birds increased. Although it could be argued that birds are not disease reservoirs and could play a zoo-prophylactic function, as it has been referred for cattle, 13 this is not supported by our results. These data suggest that bird blood attracted the transmitting sandflies and caused them to invade the house, thereby exposing the people living there to vector bites, 14,15 increasing the chance of transmission.

The association of ACL occurrence with bird-rearing in the house, even after adjusting for other variables, was a finding that, to some extent, was unexpected. Previous studies had already shown that some species of vectors were attracted by poultry blood. Massará and others 15 and Afonso and others 14 described the presence of poultry blood in the digestive tract of sandflies that were captured, respectively, in henhouses or inside the house. Although these studies did not identify whether the blood came from domestic poultry reared in the area surrounding the household or from small birds, it is plausible to suppose that the latter may be the main suppliers of blood for some sandfly species in their natural environment, and that this habit may have been transposed to the interior of houses. If this finding is true, prohibition of the rearing of these birds may contribute toward reducing the incidence of this disease. It is important to emphasize that most bird-rearing involves wild birds and that the current Brazilian environmental legislation already prohibits this practice. Nevertheless, the rearing of wild birds is a deep-rooted cultural practice among rural populations in our setting, which makes it difficult for the population to comply with this legislation. Other studies could be conducted with the aim of gaining a better understanding of the feeding habits of vectors in our environment.

It was observed among the community controls that the presence of dogs or cats outside of the house was a protection factor against acquiring ACL. At first glance, it might be supposed that these animals were a greater attraction for the vectors, which thus would bite humans less often. This reasoning may not be true, taking into consideration that this association was not observed among the neighborhood controls. Other environmental factors involved in ACL transmission may have distorted the results. The role of domestic dogs as a reservoir for ACL has been exhaustively studied, but so far no consensus has been reached. 16

Domestic animals have a variety of influences on ACL. They may become reservoirs of the parasite, thus participating in the transmission chain and increasing the risk of ACL. In this study, during the data collection, dogs and horses with suspected ACL lesions were found, and there was an association between ACL and the presence of horses (data not shown), dogs, and cats reared outside of the house. Through the attraction of these animals, these insects may come into the areas surrounding houses or inside houses and may also bite humans, and thus transmit ACL. However, these same animals may attract the vectors and thus would perform a protective role such that humans would avoid being bitten. So far, the Brazilian Ministry of Health2 does not recognize that domestic animals are participants in the transmission chain, even when infected.

Among the socioeconomic variables, to correlate those that have a closer relationship with ACL, a model containing sociodemographic variables and variables relating to the household was constructed. Among the neighborhood controls, statistically significant associations were found with absence of a gas stove, family income greater than or equal to one minimum salary, and more than 4 years of schooling. Among the community controls, the fit observed was with absence of a gas stove, non-durable wall material in the house, and per capita family income greater than US$ 28.31, which all increased the chance of acquiring ACL.

Another multivariate model brought together the factors directly relating to ACL transmission, i.e., work or school activities, leisure activities and activities outside of the house, and those relating to the area surrounding the household and the environment. It was observed that, in relation to the neighborhood controls, the risk was greater for situations of rural work or school activity, leisure activities in the forest, forest less than 200 m from the house, and bird-rearing in the house. Thus, ACL was found to be associated with three categories of variables: professional activities, leisure activities, and the area surrounding the household and the environment. In relation to the community controls, the variables relating to the areas surrounding the household and the environment that were in the previous model remained in the same multivariate model. This shows the strength of the association of these variables for this control group.7

In this study, although ACL was found to be associated with activities in the forest such as leisure activities, other indicators for transmission in the areas surrounding the household and inside the house were more marked. It was observed that several members of the same family would become ill within a short period of time and that there were a high percentage of children (15.3%) with ACL; in addition, there was an association with proximity of the forest to the home and with domestic animals inside the house and in the area surrounding the household. These findings reinforce the rural or urban fringe pattern of n transmission.2 Similar data were seen in analytical studies carried out in Argentina, despite differences in the variables that were associated with the occurrence of ACL. 7,8

From this study, the following specific control measures can be recommended: protection for individuals undertaking leisure activities in forests, distancing houses from the forest by more than 200 m, and elimination of bird or other animal-rearing inside the house. General measures of improved housing and living conditions are also recommended. These measures would certainly affect the transmission of ACL in areas of similar environmental characteristics and where ACL is endemic. Other studies should be conducted to further study the feeding habits of vectors, especially in relation to birds and domestic animals, and the role of these animals in the transmission chain of ACL.

Table 1

Multivariate analysis on the association between ACL and risk factors relating to sociodemographic variables, considering both neighbor and community controls: Alagoas, 2004–2007*

Table 1
Table 2

Multivariate analysis on the association between ACL and risk factors relating to work, school, and leisure activities and activities outside of the home, considering both neighbor and community controls: Alagoas, 2004–2007*

Table 2
Table 3

Multivariate analysis on the association between ACL and risk factors relating to the home, considering community controls: Alagoas, 2004–2007*

Table 3
Table 4

Multivariate analysis on the association between ACL and risk factors relating to the area surrounding the home and the environment, considering both neighbor and community controls: Alagoas, 2004–2007*

Table 4
Table 5

Multivariate analysis on the association between ACL and risk factors relating to sociodemographic variables and the household, considering both neighborhood and community controls: Alagoas, 2004–2007*

Table 5
Table 6

Multivariate analysis on the association between ACL and risk factors relating to work, school, and leisure activities, activities outside of the home, the area surrounding the household and the environment, considering both neighborhood and community controls. Alagoas, 2004–2007*

Table 6
Figure 1.
Figure 1.

Study population: ACL cases, Alagoas, 2004–2007.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 81, 2; 10.4269/ajtmh.2009.81.195

Figure 2.
Figure 2.

Study population: controls, Alagoas, 2004–2007.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 81, 2; 10.4269/ajtmh.2009.81.195

*

Address correspondence to Fernando de Araújo Pedrosa, Cond. Aldebaran Beta, Qd. C, Lote 2, Jardim Petrópolis, CEP: 57080-900, Maceió-AL, Brazil. E-mail: fernandopedrosa@uol.com.br

Authors’ addresses: Fernando de Araújo Pedrosa, Cond. Aldebaran Beta, Qd. C, Lote 2, Jardim Petrópolis, CEP: 57080-900, Maceió-AL, Brazil, E-mail: fernandopedrosa@uol.com.br. Ricardo Arraes de Alencar Ximenes, Departamento de Medicina Tropical, Bloco A do Hospital das Clínicas, Av. Prof. Moraes Rego s/n, Cidade Universitária, Recife-PE, Brazil, CEP 50570-420, E-mail: ricardo.ximenes@pq.cnpq.br.

Financial support: This study was supported by the Research Support Fund of the State of Alagoas (FAPEAL), Ministry of Health, National Scientific and Technological Development Council (CNPq) and Executive Health Department of the State of Alagoas (Procedure number 008/2004-PPSUS-AL).

REFERENCES

  • 1

    World Health Organization, Leishmaniasis. Geneva, WHO. Available at: http://www.who.Int/leishmaniasis. Accessed August 10, 2007.

  • 2

    Brasil, Ministério da Saúde, Secretaria de Vigilância à Saúde, 2007. Manual de Vigilância da Leishmaniose Tegumentar Americana. Second edition. Brasília, DF.

  • 3

    Alacais A, Abel L, David C, Torrez ME, Flandre P, Dedet JP, 1997. Risk factors for onset of cutaneous and mucocutaneous leishmaniasis in Bolivia. Am J Trop Med Hyg 57 :79–84.

    • Search Google Scholar
    • Export Citation
  • 4

    Davies CR, Llanos-Cuentas EA, Campos P, Mange J, Villaseca P, Dye C, 1997. Cutaneous leishmaniasis in the Peruvian Andes: risk factors identified from a village cohort study. Am J Trop Med Hyg 56 :85–95.

    • Search Google Scholar
    • Export Citation
  • 5

    Chaves LF, Cohen JM, Pascual M, Wilson ML, 2008. Social exclusion modifies climate and deforestation impacts on a vector-borne disease. PLoS Negl Trop Dis 2 :e176.

    • Search Google Scholar
    • Export Citation
  • 6

    Ampuero J, Urdaneta M, Macêdo VO, 2005. Factores de riesgo para la transmission de leishmaniasis cutánea em niños de 0 a 5 años en un área endémica de Leishmania (Viannia) brasiliensis. Cad Saude Publica 21 :161–170.

    • Search Google Scholar
    • Export Citation
  • 7

    Sosa-Estani S, Segura EL, Gómez A, Salomón OD, Peralta M, Coutada V, Ruiz LM, 2001. Leishmaniose cutânea no Norte da Argentina. Fatores de risco identificados num estudo caso-coorte em três municípios de Salta. Rev Soc Bras Med Trop 34 :511–517.

    • Search Google Scholar
    • Export Citation
  • 8

    Yadon ZE, Rodrigues LC, Davies CR, Quigley MA, 2003. Indoor and peridomestic transmission of American cutaneous leishmaniasis in northwestern Argentina: a retrospective case-control study. Am J Med Hyg 68 :519–526.

    • Search Google Scholar
    • Export Citation
  • 9

    Instituto Arnon de Melo, 2006. Enciclopédia Municípios de Alagoas. Maceió, AL.

  • 10

    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.

    • Search Google Scholar
    • Export Citation
  • 11

    Lins ALGO, 1996. Leishmaniose tegumentar de americana—estudo epidemiológico em Pernambuco no período 1985–1994. Master dissertation. Recife-PE: Universidade Federal de Pernambuco.

  • 12

    Aguiar GM, Medeiros WM, 2003. Distribuição e habitat. Rangel EF, Lainson R, eds. Flebotomíneos de Brasil. Fiocruz, 207–256.

  • 13

    Bern C, Hightower AW, Chowdhury R, Ali M, Amann J, Wagatsuma Y, Haque R, Kurkjian K, Vaz LE, Begum M, Akter T, Cetre-Sossah CB, Ahluwalia IB, Dotson E, Secor WE, Breiman RF, Maguire JH, 2005. Risk factors for kala-azar in Bangladesh. Emerging Infectious Diseases. Volume 11. Available at: www.cdc.gov/eid. Accessed September 15, 2007.

  • 14

    Afonso MMS, Gomes AC, Meneses CRV, Rangel EF, 2005. Studies on the feeding habits of Lutzomyia (N) intermedia (Diptera, Psychodidae), vector of cutaneous leishmaniasis in Brazil. Cad Saude Publica 21 :1816–1820.

    • Search Google Scholar
    • Export Citation
  • 15

    Marassá AM, Consales CA, Galati EAB, Nunes VLB, 2006. Identificação do sangue ingerido por Lutzomyia (Lutzomyia) longipalpis (Lutz & Neiva, 1912) e Lutzomyia (Lutzomyia) almeriori (Galati & Nunes, 1999) pela técnica imunoenzimática do ELISA de captura, no sistema avina-biotina. Rev Soc Bras Med Trop 29 :183–186.

    • Search Google Scholar
    • Export Citation
  • 16

    Reithinger R, Davies CR, 1999. Is the domestic dog (Canis familiaris) a reservoir host of American cutaneous leishmaniasis? A critical review of the current evidence. Am J Med Hyg 61 :530–541.

    • Search Google Scholar
    • Export Citation
Save