Onicio Batista Leal NetoI; Thiago Yury Cavalcanti GalvãoII; Fabrício Andrade Martins EstevesIII; Ayla Maritcha Alves Silva GomesII; Elainne Christinne de Souza GomesI, III; Karina Conceição Gomes Machado de AraújoIV; Constança Simões BarbosaI
IAggeu Magalhães Research Center of the Oswaldo Cruz Foundation (CPqAM-FIOCRUZ/PE)
IICaruaruense Association of Higher Education (ASCES)
IIIVitória Academic Center (CAV-UFPE)
IVFederal University of Sergipe
The objective of this study was to describe the spatial distribution of schistosomiasis in horticultural community of Natuba, district of Vitória de Santo Antão, Pernambuco state. It was conducted a parasitological survey, examined the fecal material of 310 community residents. The cases positive for Schistosoma mansoni were geocoded and included in the computerized template of the community, generating maps of spatial distribution with kernel estimators. The results showed a high prevalence of schistosomiasis, with 28.4% of the parasites. Other parasites were found in 25.8% of the population. The use of GIS tools to map and understand the possible distribution of cases of schistosomiasis in the space occupied by the community highlighting and listing locations of lower elevation (able to flooding), with a higher frequency of human cases. Studies like this provide information to the local health services, may intervene and bring about change for individuals living in areas with low housing conditions to minimize their exposure to risk of contracting schistosomiasis.
Keywords: Schistosomiasis. Spatial analysis. Epidemiology. Public Health.
Brazil, a developing country, has public health problems due to the lack of policies oriented toward health promotion and education and due to the low investments in basic and environment sanitation, leading to not very healthy spaces for less privileged populations. Certain infectious-parasitic diseases are still quite widespread and have high prevalence rates in this socio-environmental setting1-6. Endemic diseases such as schistosomiasis mansoni are chronic in individuals infested at sites where the health status is a manifestation of unhealthy environments7. The space-time approach considers that sites have historical, social and political inheritances, and thus persisting endemic diseases may be represented by risky cultural practices molded throughout a long process of absence of health care8.
By trying to understand the relationship between environment and health, the studies that approach the theme have successfully used geoprocessing tools to analyze hazards spatially, trying to assess the impact of adverse environmental conditions on the integrity of individuals in time and space9. Geoprocessing is a set of techniques to collect, show and treat spatial information, used along with Geographical Information System (GIS) and Global Positioning System (GPS) tools to develop appropriate models for the surveillance, forecast and prevention of risks for diseases10. Using maps has shown to be the best form of representation, as it gives the researcher an immediate and direct vision of the distribution of an event in space. Moreover, by using GIS, it is easier to check any spatial associations between health events and different aspects of the natural and built environment11.
The World Health Organization (WHO) underscores the importance of identifying foci of transmission of diseases in environments of high prevalence and/or incidence of parasite infections, generating information to substantiate and support the implementation of health education programs capable of minimizing risks1,12,13. The search and identification of potential foci of parasite infections are extremely important to public health, given they can provide prophylactic and educational information to fight the forms of transmission and development of these conditions, mainly in regions where schistosomiasis is historically endemic, such as the Zona da Mata of Pernambuco, where several control strategies been thought of, although no advance has been sustainable enough for its control14-17.
The present study aimed to describe the occurrence of parasite infections in the community of Natuba in Vitória de Santo Antão, Pernambuco, relating age group and work activity. Trying to evaluate the expression of schistosomiasis at the site through spatial analysis (spatial distribution, Kernel estimator and analysis of altimetry) was particularly pursued, given the location has had a scenario prone to the introduction and maintenance of the biological cycle of the Schistosoma mansoni for decades.
A cross-sectional analytical study was performed between October 2008 and March 2009 at the vegetable farming community of Natuba, district of the municipality of Vitória de Santo Antão-PE, located in the Zona da Mata of the state of Pernambuco, 45.1 kilometers from Recife, with a population of 896 inhabitants8. The referred community is crossed by the Natuba River, downstream to the South portion of the community, part of the Tapacurá water basin. River waters are used to irrigate and support daily household activities, such as washing clothes and leisure for the community. The climate is hot and humid, with an annual average temperature of 24.6ºC. The main route of access is the BR-232, a road of great economic importance for the state of Pernambuco. The vegetables grown by the community are sold at road sides and are also distributed to the markets of neighboring cities, making it one of the largest vegetable producing poles of the State of Pernambuco. The population of this region is in daily contact with the waters of this spring that harbors the snail vectors of this disease, due to work and daily activities. Therefore, most individuals are exposed to the risks of acquiring schistosomiasis and continuing its cycle.
The coproscopy survey was done by sampling, covering the entire community. EpiInfo 3.5.1 was used to calculate the minimum sample necessary to obtain results with statistical significance, with a 35% estimated prevalence and a maximum error of 5% for schistosomiasis in the community, based on a previous study15. A minimum number of 284 patients was established for a 95% level of confidence. Aimed at guaranteeing the reliability of results and minimizing the risk of bias due to sample loss, coproscopy was performed in 310 community dwellers.
The material for coproscopy was stored in a thermal box at 8ºC and transported to the Parasitology laboratory of the Associação Caruaruense de Ensino Superior - ASCES/FAAPE for processing. Parasitology feces tests were performed using two techniques, Hoffmann, Pons & Janner19 and Kato-Katz20, for each patient. Patients with any kind of parasite were duly referred for treatment. All households with cases of schistosomiasis were used for georeferencing for thematic and analytical maps.
A malacological survey was performed, electing the ridges of vegetable gardens as the site of highest exposure of farmers, given pools of Biomphalaria straminea were found. Graspers were used at the collecting stations marked at the ridges of the vegetable gardens, where all visible snails were captured. Collecting stations were georeferred by the Global Positioning System (GPS).
In order to identify the height of the flooded points, an altimetry resource of the GPS platform Garmin, eTrex model was used. All flood limits were marked, based on the visual recognition of field surveyors and on the report of community dwellers. In order to make the location sketch, a method described by The National Health Foundation (FUNASA)21 was used, according to the Geographical Indication guide. Group technicians systematically went through the community making the digital design of the locality. Data were transferred from the GPS to the computer and processed by GPS TrackMaker PRO software to correct polygons on the computerized template and to adjust for the virtual spectrum generated by trails. The river network map was purchased at the Pernambuco Technology Institute (ITEP). After treatment, points, lines and polygons were imported to the ArcGIS version 10(ESRI) software, where spatial analysis was performed. Descriptive data were analyzed by the EpiInfo 3.5.1 statistical package, using a p-value of 0.05 with a 95% confidence interval.
The Kernel estimator, a non-parametric technique that promotes statistical suavization generating chromatic gradients with "hot spots", was adopted for spatial analysis and identification of patterns of distribution and density of cases, given it concentrates the density of cases in a certain area. The gradient level is controlled by choosing a parameter known as band width (in the present study, 200 meters for positive cases), which indicates the area to be considered in the calculation and should reflect the geographical scale of the assumption of interest, and the previous knowledge on the event studied. The Kernel Polynomial 5 Interpolation with barriers technique, capable of generating chromatic intensity gradients was used for the interpolation between the dependent variable (case) and the geographical variable (elevation).
The study was registered at the Ethics in Research Committee of Associação Caruaruense de Ensino Superior (CEP/ASCES), approved by letter ACP nº155/08 CEP/ASCES. Volunteer participation of dwellers of the farming region included in the study was confirmed by the signature of the Consent Form.
Of the 310 individuals analyzed, 190 (61.3%) had at least one parasite, S.mansoni having been the most frequent species, with a 28.4% frequency in the population studied (Table 1). The mean parasite load for S. mansoni in these individuals was 60.2 eggs per gram of feces (opg), ranging between 24 and 408 opg.
Polyparasitism was observed in 25.8% of the population studied, 58.7% of which with two parasites, 25% with three parasites and 16% with four parasites. Among age groups, the age group between 10-19 and 20-29 years was affected most, with 29.6% of individuals infected by S. mansoni (Table 2). No significant differences were observed between the proportion of men and women infected.
Forty-three samples of snails of the Biomphalaria straminea species were collected during the malacological survey on the ridges of vegetable gardens. After the specimens were exposed to an artificial light source (60 w bulb) for 2 hours, the elimination of S. mansoni cercariae was not observed. Other species of snails at capture sites such as Melanoides tuberculatus and Pomacea sp. were also detected.
The computerized template of the location (Figure 1) shows the distribution of vegetable gardens and of Biomphalaria pools. Figure 2 shows the concentration of positive cases for S. mansoni in the community. Figure 3 has an interpolation map of cases with the elevation, which is related to the flood area highlighted at the location.
In Natuba, the site built by the community for economic support is represented by a vast extension of vegetable gardens with irrigation ridges, a system that represents 75% of the local area. Vegetable gardens are irrigated with water extracted from the river by suction pumps and sprinkling hoses carry and spread the vector snails throughout the plantation. As the gardens are irrigated constantly, their side ridges are always soaked in water, forming excellent artificial pools where snails find food (lettuce waste) and reproduce themselves abundantly.
In 1998, Barbosa CS & Barbosa FS15 had already registered that sanitary sewages from most homes drained into the Natuba River, leading to the contamination of the water environment, favoring the establishment and maintenance of the cycle of parasites like S. mansoni. The present study observed that the same sanitation and environment conditions remain and modulate the current local epidemiological landscape.
The flooding of the ridges where vegetables are cultivated creates the necessary and ideal conditions for the survival of B. straminea. Although this snail is considered a bad biological host for S. mansoni, as the exposure of farmers is intense and systematic, and due to their work activity, it guarantees the high prevalence and maintains the intensity of the infection in the community.
The non-shedding of cercariae in the lab from snails collected may be explained by the low susceptibility of this vector species22.
A previous study performed at this location15 registered 35.1% of the population infected by S. mansoni. On that occasion, all cases received specific medication for treatment. The population of Natuba can be considered stable, as it has owned the land for decades. And the fact that the present study diagnosed a prevalence of 28.4% means that the epidemiological pattern of contamination of the environment and infection also is stable, in face of the observation of the maintenance of the unhealthy environment and working conditions that promote the maintenance of cases of schistosomiasis and guarantee the chronicity of the disease in the community.
The occurrence of a higher number of cases of the disease in young adults may be related to their work, given that this age group is more productive and, consequently more exposed, which can be corroborated by other studies23,24. On the other hand, schoolchildren (regardless of gender) were observed to be more exposed to activities related to using river water for leisure. The transmission model found in Natuba is similar to those identified in studies that approach eco-epidemiology, in which the understanding of the disease cannot be dissociated from the analysis of the space in which the individual is inserted25. The polyparasitism shown in the present study can be understood in a similar way to previous studies26-28, in which there are the characteristics of living conditions and routine of individuals that live at sites with precarious sanitary conditions.
The theme map presented by Figure 2 shows that most individuals infested by the S. mansoni live in the north region of the location. In this region, there are important water collections that are potential natural pools for Biomphalaria, although they were not found there. The location of individuals infected near these rivers represents a favorable setting for the expansion of schistosomiasis to the site and to neighboring areas, putting in risk a part of the population living there and not comprised of farmers.
Figure 3 associates the distribution of cases with the geographical elevation variable, showing that the areas with lower elevations concentrate the highest number of cases because they are more susceptible to flooding by the overflow of the Natuba River during the rainy seasons, enabling contact of individuals with water and increasing the risk for schistosomiasis infection. This seasonal and occasional event probably represents a less important impact on the transmission of the disease than the daily exposure of farmers in the pools of the vector snails detected in the gardens.
In general, using geotechnologies for building epidemiological settings is of great value for diseases such as schistosomiasis, that have a major environmental component in the understanding of their transmission29,30.
The results of the present study indicate that the transmission of schistosomiasis at this site has remained throughout the years due to the geographical structure and work activities of the population, associated with the precarious sanitation conditions. Based on what was exposed, interventions for interrupting the transmission cycle should be based on improvements in sanitation and in the environment, such as basic sanitation and drainage of rain water, given the impossibility and inconvenience of promoting changes in the physical structure or in the work model of the community without affecting the local economy and disturbing the social order established there.
Acknowledgements: To the Health Department of Vitória de Santo Antão, in the person of Francisco Santos, to the health community agents of the Family Health Center of Natuba and to technician Valdeci Oliveira for his contribution to field activities.
1. Carmo HE, Barreto ML. Esquistossomose mansônica no estado da Bahia, Brasil: Tendências histórias e medidas de controle. Cad Saúde Pública 1994. 10(4): 425-39.
2. Ludwig KM, Frei F, Filho FA, Ribeiro-Paes JT. Correlação entre condições de saneamento básico e parasitoses intestinais na população de Assis, Estado de São Paulo. Rev Soc Bras Med Trop 1999; 32(5): 547-55.
3. 'Machado ER, Santos DS, Costa-Cruz JM. Enteroparasites and commensals among children in four peripheral disctricts of Uberlândia, State of Minas Gerais. Rev Soc Bras Med Trop 2008; 41(6): 581-5.
4. Machado MT, Machado TMS, Yoshikae RM, Schimidt ALA, Faria RCA, Paschoalotti MA et al. Ascariasis in the subdistrict of Cavacos, municipality of Alterosa(MG), Brazil: Effect of mass treatmente with albendazole on the intesity infection. Rev Inst Med Trop 1996; 38(4): 265-71.
5. Rocha RS, Silva JG, Sérgio VP, Caldeira RL, Firmo JOA, Carvalho OS et al. Avaliação da esquistossomose e de outras parasitoses intestinais, em escolares do município de Bambuí, Minas Gerais, Brasil. Rev Soc Bras Med Trop 2000; 33(5): 431-6.
6. Tavares-Dias M, Grandini AA. Prevalência e aspectos epidemiológicos de enteroparasitoses na população de São José da Bela Vista, São Paulo. Rev Soc Bras Med Trop 1999; 32(1): 63-5.
7. Souza MAA, Barbosa VS, Wanderlei TNG, Barbosa CS. Criadouros de Biomphalaria, temporários e permanentes, em Jaboatão dos Guararapes, PE. Rev Soc Bras Med Trop 2008; 41(3): 252-6.
8. Barcellos C et al: Organização espacial, saúde e qualidade de vida: análise espacial e uso de indicadores na avaliação de situações de saúde. Inf Epidemiol Sus 2002; 11(3).
9. Barcellos C, Bastos FI. Geoprocessamento, ambiente e saúde: Uma união possível? Cad Saúde Pública 1996; 12(3): 389-97.
10. Rodrigues M. Introdução ao geoprocessamento. In: Simpósio Brasileiro de Geoprocessamento. São Paulo: Sagres Editora; 1990.
11. Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Fundação Oswaldo Cruz. Sistemas de Informações Geográficas e Análise Espacial na Saúde Pública. Ministério da Saúde, Fundação Oswaldo Cruz. Brasília: Ministério da Saúde; 2007.
12. Guerra EM, Vaz AJ, Toledo LAS, Ianoni AS, Quadros CMS, Dias RMDS et al. Infecções por helmintos e protozoários intestinais em gestantes de primeira consulta atendidas em centros de saúde da rede estadual no subdistrito do Butantã, município de São Paulo. Rev Inst Med Trop 1991; 33(4): 303-8.
13. Pordeus LC, Aguiar LR, Quinino LRM, Barbosa CS. A ocorrência das formas aguda e crônica da esquistossomose mansônica no Brasil no período de 1997 a 2006: uma revisão de literatura. Epidemiol Serv Saúde 2008; 17(3): 163-75.
14. Barbosa CS, Araújo KC, Antunes L, Favre T, Pieri OS. Spatial distribution of Schistosomiasis foci on Itamaracá island, Pernambuco, Brazil. Mem Inst Oswaldo Cruz 2004; 99(1): 79-83.
15. Barbosa CS, Barbosa FS. Padrão epidemiológico da esquistossomose em comunidade de pequenos produtores rurais de Pernambuco, Brasil. Cad Saúde Pública 1998; 14(1): 129-37.
16. Carvalho EMF, Acioli MD, Branco MAF, Costa AM, Cesse EAP, Andrade AG et al. Evolução da esquistossomose na zona da mata sul de Pernambuco. Epidemiologia e situação atual: controle ou descontrole? Cad Saúde Pública 1998. 14(4): 787-95.
17. Fontbonne A, Freese-de-Carvalho E, Acioli MB, Sá GA, Cesse EAP. Fatores de risco para poliparasitismo intestinal em uma comunidade indígena de Pernamuco, Brasil. Cad Saúde Pública 2001; 17(2): 367-73.
18. Instituto Brasileiro de Geografia e Estatística. Censo 2010. Disponível em http://www.ibge.gov.br. [Acessado em 18 de janeiro de 2011] .
19. Hoffman WA, Pons JA, Janer JL. Sedimentation concentration method in schistosomiasis mansoni. Puerto Rico. J Pub Health 1934; 9: 283-98.
20. Kato K, Miura M. Comparative examinations. Japan J Parasitol 1954; 3: 35.
21. Fundação Nacional de Saúde. Manual de Reconhecimento Geográfico da Fundação Nacional de Saúde - FUNASA; 1996.
22. Kuntz ER. Effect of light and temperature on shedding of Schistosoma mansoni cercarie. Naval Med Res Inst 1946; 7:16.
23. Martins Jr. DF, Barreto ML. Aspectos macroepidemiológicos da esquistossomose mansônica: análise da relação da irrigação no perfil espacial da endemia no estado da Bahia, Brasil. Cad Saúde Pública 2003. 19(2): 383-93.
24. Vasconcelos CH, Cardoso PCM, Quirino WC, Massara CL, Amaral GL, Cordeiro R et al. Avaliação de medidas de controle da esquistossomose mansoni no município de Sabará, Minas Gerais, Brasil, 1980-2007. Cad Saúde Pública 2009; 25: 997-1006.
25. Ariza E et al. Eco-epidemiología: El futuro posible de La epidemiologia. Rev La Fac Nac Salud Publica 2004; 22(1): 139-45.
26. Fontbonne A, Freese-de-Carvalho E, Acioli MD, Sá GA, Cesse EAP. Fatores de risco para poliparasitismo intestinal em uma comunidade indígena de Pernambuco, Brasil. Cad Saúde Pública 2001; 17(2): 367-73.
27. Agudelo-Lopez S, Gómez-Rodríguez L, Coronado X, Valencia-Gutierrez CA, Restrepo-Betancur LF, Galvis-Gómez LA et al. Prevalencia de Parasitosis Intestinales Factores Asociados en un Corregimiento de la Costa Atlántica Colombiana. Rev Salud Pública 2008; 10(4): 663-64.
28. Santos SA & Merlini LS. Prevalência de enteroparasitoses na população do município de Maria Helena, Paraná. Ciênc Saúd Coletiva 2010; 15(3): 899-905.
29. Xu B, Gong P, Biging G, Liang S, Seto E, Spear RC. Snail density prediction for schistosomiasis control using Ikonos and Aster images. Photogramm Eng Rem Sens 2004; 70 (1): 1285-94.
30. Raso G, Vounatsou P, Singer BH, Goran EKN, Tanner M, Utzinger J. An integrated approach for risk profiling and spatial prediction of Schistosoma mansoni-hookworm coinfection. Proc Nat Acad Sci 2006; 103: 6934-9. Correspondence to: Received: 09/08/11
Onicio Batista Leal Neto
Centro de Pesquisas Aggeu Magalhães, Serviço de Referência em Esquistossomose.
Av. Professor Moraes Rego s/n, Cidade Universitária,
Recife, PE, Brasil CEP 50670-420
Final version: 25/06/12
Disclosure: All authors declare no conflicts of interest.