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Schistosomiasis in the Middle Paranapanema river region, state of São Paulo, Brazil: Does it matter today for public health?

Abstract

INTRODUCTION:

The Middle Paranapanema watershed is known for the transmission of schistosomiasis, and there have been autochthonous cases since 1952. This study aimed to describe this disease in space and time and evaluate its current importance as a public health problem.

METHODS:

Thematic maps showing the risk areas for transmission of schistosomiasis, using scan statistics, and flow maps were created in the period 1978-2016. Incidence was calculated, and the existence of spatial dependence between autochthonous and imported cases was evaluated using Ripley’s K12-function. Species of snails were identified in high-risk clusters.

RESULTS:

A total of 1,511 autochthonous cases were reported in eight of the 25 municipalities in the study area, of which 92.8% occurred in Ourinhos. A total of 2,189 imported cases were reported (27% in Ourinhos and 20% in Assis), mainly originating in the states of Paraná and Minas Gerais. Clusters of autochthonous and imported cases with higher risk were identified in Ourinhos, Assis and Ipaussu. However, over the years, the cases began to occur in low density in Ourinhos and no longer in other municipalities in the region. The cluster detected in the period 2007-2016 in Ourinhos still has risk for the transmission of schistosomiasis. K12-function analysis indicated positive spatial dependence between autochthonous and imported cases.

CONCLUSIONS:

The study showed that, currently, schistosomiasis as a public health problem in Middle Paranapanema is restricted to Ourinhos. This fact may be related to the presence of Biomphalaria glabrata at a specific point and low coverage of basic sanitation.

Keywords:
Schistosomiasis; Spatial analysis; Geocoding; Epidemiology; Brazil

INTRODUCTION

Human schistosomiasis mansoni is a parasitic disease in which the etiological agent is the trematode Schistosoma mansoni Sambon, 1907. The disease occurs in areas where there is poor sanitation, the intermediate host (IH) of the genus Biomphalaria can be found, and where infected people with schistosomiasis migrate to non-endemic regions while healthy people to endemic regions, all of which are factors that favor the emergence of the disease11. Rollemberg CVV, Santos CMB, Silva MMBL, Souza AMB, Silva ÂM, Almeida JAP, et al. Aspectos epidemiológicos e distribuição geográfica da esquistossomose e geo-helmintos, no Estado de Sergipe, de acordo com os dados do Programa de Controle da Esquistossomose. Rev Soc Bras Med Trop. 2011;44(1):91-96.,22. Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. The Lancet 2014;383(9936);2253-2264.. It was reported that, in 2016, 12,411 adults were treated, and approximately 1.6 million individuals were infected with S. mansoni (Sm) in Brazil33. World Health Organization (WHO). Schistosomiasis and soil-transmitted helminthiases: number of people treated in 2016. Weekly Epidemiological Record: WHO; 2017. 92(49):749-760 p.,44. World Health Organization (WHO). Schistosomiasis: status of schistosomiasis endemic countries: 2017. WHO; 2018 [updated 2018]. Available from: http://www.who.int/neglected_diseases/ntddata/sch/sch.html.
http://www.who.int/neglected_diseases/nt...
. In 2012, positivity for Sm in Brazil was 4.5%55. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: diretrizes técnicas. 4a edição. Brasília: MS; 2014. 13-20 p.. In 2015, there was a decrease in positivity, to 1% in Brazil, with 2.4% in the southeast region and 0.04% in São Paulo (SP)66. Katz N. Inquérito Nacional de Prevalência da Esquistossomose mansoni e Geo-helmintoses. Belo Horizonte: CPqRR; 2018. 76 p..

Knowledge of spatial variation and geographical mapping of schistosomiasis cases allow identification of areas where there is a greater risk of infection and determination of priority areas for prevention measures55. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: diretrizes técnicas. 4a edição. Brasília: MS; 2014. 13-20 p.. Geographical information systems (GISs) have been used in public health studies since the 1990s and allow large quantities of data to be analyzed and disease transmission risks in a particular geographical area to be identified77. Medronho RDA. Geoprocessamento e saúde: uma nova abordagem do espaço no processo saúde doença. Rio de Janeiro: FIOCRUZ/CICT/NECT; 1995.

8. Vine MF, Degnan D, Hanchette C. Geographic Information Systems: Their use in environmental epidemiologic research. Environ Health Perspect. 1997;105:598-605.

9. Organización Panamericana de la Salud (OPS). Uso de los Sistemas de Información Geográfica en Epidemiología (SIG-EPI), Bol Epidemiol. 1996;17(1):1-6.

10. Carvalho MS, Pina MF, Santos SM. Conceitos Básicos de Sistemas de Informação Geográfica e Cartografia Aplicados à Saúde. Brasília. Organização Panamericana de Saúde, Ministério da Saúde. 2000; 124 p.

11. Carvalho MS, Souza-Santos R. Analysis of spatial data in public health: methods, problems, and perspectives. Cad Saude Publica. 2005;21(2):361-78.

12. Austin MP. Spatial prediction of species distribution: an interface between ecological theory and statistical modelling. Ecological modelling. 2002;157(2):101-18.
-1313. Waller LA, Gotway CA. Applied Spatial Statistics for Public Health Data. New Jersey: John Wiley & Sons; 2004. 520 p..

In Brazil, GISs have been used in studies to evaluate the occurrence of schistosomiasis, taking into account the geographical space, particularly in areas of high endemicity in Bahia1414. Bavia ME, Hale LF, Malone JB, Braud DH, Shane SM. Geographic information systems and the environmental risk of schistosomiasis in Bahia, Brazil. Am J Trop Med Hyg. 1999;60(4):566-72.-1515. Cardim LL, Ferraudo AS, Pacheco STA, Reis RB, Silva MMN, Carneiro DDMT, et al. Análises espaciais na identificação das áreas de risco para a esquistossomose mansônica no município de Lauro de Freitas, Bahia, Brasil. Cad Saude Publica . 2011;899-908., Pernambuco1616. Gomes E, Leal-Neto OB, Albuquerque J, da Silva H, Barbosa CS. Schistosomiasis transmission and environmental change: a spatio-temporal analysis in Porto de Galinhas, Pernambuco-Brazil. Int J Health Geogr. 2012;11(1):51., Minas Gerais1717. Guimarães RJ, Fonseca FR, Dutra LV, Freitas CC, Oliveira GC, Carvalho OS. A study of Schistosomiasis prevalence and risk of snail presence spatial distributions using geo-statistical tools. In Schistosomiasis. Prof Mohammad Bagher Rokni (Ed.) InTech. 2012;255-80.-1818. Fonseca F, Freitas C, Dutra L, Guimarães R, Carvalho O. Spatial modeling of the Schistosomiasis mansoni in Minas Gerais State, Brazil using spatial regression. Acta Trop. 2014;133:56-63., Recife1919. Barbosa CS, Barbosa VS, Nascimento WC, Pieri OS, Araujo KCGM. Study of the snail intermediate hosts for Schistosoma mansoni on Itamaracá Island in northeast Brazil: spatial displacement of Biomphalaria glabrata by Biomphalaria straminea. Geospat Health. 2014;8:345-351., and Sergipe2020. Santos ADD, Lima ACR, Santos MB, Alves JAB, Góes MADO, Nunes MAP, et al. Spatial analysis for the identification of risk areas for schistosomiasis mansoni in the State of Sergipe, Brazil, 2005-2014. Rev Soc Bras Med Trop . 2016;49(5):608-15.. Studies in areas with low endemicity of schistosomiasis, such as the state of SP, are rare. The studies by Anaruma Filho et al.2121. Anaruma-Filho F, Sant'Ana JM, dos Santos RF, Castagna CL. Environmental inducers of Schistosomiasis mansoni in Campinas, Brazil. Geospat Health . 2010;5(1):79-91. and Teles et al.2222. Teles HMS, Ferreira CS, Carvalho MED. Assessment of control and epidemiologic details of the schistosomiasis mansoni in Bananal, São Paulo, Brazil. Rev Bras Epidemiol. 2014;17:531-42. show an exception, relating to Bananal and Campinas, respectively, regions where it was possible to rate schistosomiasis transmission sites, map parasite foci, and identify those where intense surveillance and control would be required.

The Middle Paranapanema watershed, in SP, stands out as an important region for the transmission of schistosomiasis, with the occurrence of autochthonous cases since 1952.2323. Ferreira JM, Meira JA. Três casos de esquistossomose mansoni procedentes do interior do Estado de São Paulo (Ourinhos, Palmital e Ipauçu). Foco autóctone na cidade de Ourinhos. Rev Paul Med. 1952;41(1):15-8. Among the factors that could explain this autochthony would be the predominance and abundance of Biomphalaria glabrata.2424. Piza JDT, Ramos ADS, Moraes LDC, Corrêa RDR, Takaku L, Pinto ADM. Carta planorbídica do Estado de São Paulo. Secretaria de Estado da Saúde, Campanha de Combate à Esquistossomose (CACEsq) São Paulo, 1972.

25. Teles HMS, Vaz JF. Distribuição de Biomphalaria glabrata (Say, 1818) (Pulmonata, Planorbidae) no estado de São Paulo, Brasil. Rev Saude Publica. 1987;21(6):508-12.

26. Teles HMS. Distribuição geográfica das espécies dos caramujos transmissores de Schistosoma mansoni no Estado de São Paulo. Rev Soc Bras Med Trop . 2005;38(5):426-32.
-2727. Tuan R. Diversity and distribution of the Biomphalaria species in the middle reaches of the Paranapanema River, São Paulo, SP, Brazil. Biota Neotrop. 2009;9(1):279-283. This species was found naturally infected with Sm for the first time in 1952 in Ourinhos.2828. Rey L. Primeiro encontro de planorbídeos naturalmente infestados por furcocercárias de S. mansoni no planalto paulista (Ourinhos). Rev Clín Sao Paulo. 1952;28:57-64.-2929. Magalhães LA, Dias LCS. Estudo da suscetibilidade da Biomphalaria glabrata de Ourinhos (SP), à infecção pelo Schistosoma mansoni de Belo Horizonte (MG), e de São José dos Campos (SP). Rev Saude Publica . 1973;7(3):295-7. It has since been considered an important public health problem in this area of the state3030. Chieffi PP, Waldman EA. Aspectos particulares do comportamento epidemiológico da esquistossomose mansônica no Estado de São Paulo, Brasil. Cad Saude Publica . 1988;4(3):257-75.-3131. Piza JDT, Ramos ADS, 1960. Os focos autóctones de esquistossomose no Estado de São Paulo. Arq Hig Saude Publica. 25(86):261-71.. However, in this region, as in Brazil as a whole and several other countries of the world, recently, there has been a significant decrease in the incidence and prevalence of schistosomiasis, which has been attributed to the efficacy of the drugs used for treatment of infected individuals, increase in the coverage of basic sanitation services, and control of the IH3232. Waldman EA, Silva LJ, Monteiro CA. Trajetória das Doenças Infecciosas: da Eliminação da Poliomielite à Reintrodução da Cólera. Inf Epidemiol Sus. 1999;8(3):5-47.

33. Barata RB. Cem anos de endemias e epidemias. Cien Saude Colet. 2000;5(2):333-45.

34. Organização Mundial de Saude (OMS). Trabalhando para superar o impacto global de doenças tropicais negligenciadas: Primeiro relatório da OMS sobre doenças tropicais negligenciadas. Brasília: OMS. 2010, 188 p.
-3535. World Health Organization (WHO). Schistosomiasis: progress report 2001-2011 and strategic plan 2012-2020. Geneva: WHO; 2013, 74 p..

Thus, this study aimed to describe the historical occurrence of schistosomiasis in the Middle Paranapanema region in space and time, characterize the presence of IH in areas at risk, and evaluate its current importance as a public health problem.

METHODS

The study area consists of 25 of 55 municipalities of the Hydrographic Unit Water of Resources Management of Middle Paranapanema (UGRHI-17)3636. Comitê da Bacia Hidrográfica do Médio Paranapanema (CBH-MP). Relatório de Situação dos Recursos Hídricos 2018 (Ano Base: 2017) - UGRHI-17. CBH-MP. 2018. [updated 2019]. Available from: Available from: http://cbhmp.org/publicacoes/relatorios/
http://cbhmp.org/publicacoes/relatorios/...
-3737. Comitê da Bacia Hidrográfica do Médio Paranapanema (CBH-MP). Relatório Zero Relatório de Situação dos Recursos Hídricos da UGRHI-17 | ano: 1999. CBH-MP, 1999. [updated 2019]. Available from: Available from: http://cbhmp.org/publicacoes/relatorioz/
http://cbhmp.org/publicacoes/relatorioz/...
(Table 1), including GeoSentinel sites that are priorities for the surveillance of schistosomiasis3838. Eduardo MBP. Avaliação da Esquistossomose no Estado de São Paulo. Documento técnico/Relatório de Avaliação. Secretaria do Estado da Saúde, Coordenadoria de Controle de Doenças, Centro de Vigilância Epidemiológica, Divisão de Doenças de Transmissão Hídrica e Alimenta, 2008, 59 p., which have a total estimated population of 488,955 inhabitants in 20183939. Instituto Brasileiro de Geografia e Estatística (IBGE). Estimativas de população residente nos Municípios Brasileiros com data de referência em 1º de julho de 2018. IBGE; 2018 [updated 2019]. Available from: Available from: https://www.ibge.gov.br/estatisticas-novoportal/sociais/populacao/9103-estimativas-de-populacao.html?=&t=resultados/ .
https://www.ibge.gov.br/estatisticas-nov...
. These municipalities include a significant part of the autochthonous occurrence of schistosomiasis in the Middle Paranapanema region4040. Sistema de Informação de Agravos de Notificação (SINAN). Casos confirmados por Evolução e por Autóctone Mun. Res. segundo UF Notificação [Internet]. Brasília: SINAN Net. Ministério da Saúde/SVS; 2018 [updated 2018]. Available from: Available from: http://portalsinan.saude.gov.br/sinan-net/ .
http://portalsinan.saude.gov.br/sinan-ne...
. The aforementioned region is located in the southeast of SP. It is characterized by a vast and complex hydrography in which the Paranapanema river predominates and flows into the west of SP in the direction of the Paraná River4141. Centro de Vigilância Epidemiológica (CVE). Vigilância Epidemiológica. Divisão de Doenças de Transmissão Hídrica e Alimentar. Esquistossomose - [Dados estatísticos 1981 - 2009 - definitivo] [Internet]. São Paulo: CVE; 2011 [updated 2018]. Available from: Available from: http://www.cve.saude.sp.gov.br/ .
http://www.cve.saude.sp.gov.br/...
-4242. Peron AF, Piroli EL. Projeto APPs: Conhecendo e cuidando da bacia hidrográfica do Rio Pardo. CEDIAP-GEO- Centro de Estudo e Divulgação de Informações sobre Áreas Protegidas, Bacias Hidrográficas e Geoprocessamento 1th ed. 2011. 23 p..

TABLE 1:
Autochthonous, imported, and unknown origin cases of schistosomiasis in the eight autochthonous municipalities and the sum of the cases of the other municipalities* of the GeoSentinel sites of Middle Paranapanema, state of São Paulo, Brazil, according to the four study periods (1978-2016).

Information on schistosomiasis cases (notification date, home address, probable infection site [PIS], and epidemiological classification) in the period 1978-2016 was obtained from the National Notifiable Disease Information System (SINAN). Access to the necessary information was provided by the Alexandre Vranjak Center for Epidemiological Surveillance and the Superintendence for the Control of Endemic Diseases (SUCEN) of the Health Secretariat of the State of SP. Population data and cartographic material were obtained from the information supplied by the Brazilian Institute of Geography and Statistics (IBGE)4343. Instituto Brasileiro de Geografia e Estatística (IBGE). Anuário estatístico do Brasil 1982 [Internet]. Rio de Janeiro: IBGE; 1983 [updated 2018]. Available from:Available from:http://seculoxx.ibge.gov.br/images/seculoxx/arquivos_download/populacao/1982/populacao_m_1982aeb_016_a_017.xls/ .
http://seculoxx.ibge.gov.br/images/secul...

44. Instituto Brasileiro de Geografia e Estatística (IBGE). Setor Censitário 2010. Mapas, bases e referenciais, bases cartográficas, malhas digitais, Instituto Brasileiro de Geografia e Estatística [Internet]. Brasil: IBGE; 2010 [updated 2018]. Available from: Available from: http://mapas.ibge.gov.br/ .
http://mapas.ibge.gov.br/...

45. Instituto Brasileiro de Geografia e Estatística (IBGE). Base Contínua 250 mil, Hidrografia. Mapas, Interativos, serviços, serviços do ArcGIS [Internet]. Brasil: IBGE ; 2010 [updated 2018]. Available from: Available from: http://mapas.ibge.gov.br/ .
http://mapas.ibge.gov.br/...

46. Instituto Brasileiro de Geografia e Estatística (IBGE). Estimativas populacionais para os municípios e para as Unidades da Federação brasileiros em 01.07.1994 [Internet]. Brasil: IBGE ; 2016 [updated 2018]. Available from: Available from: https://downloads.ibge.gov.br/downloads_estatisticas.htm? Caminho=/Estimativas_de_ Populacao/Estimativas_1994/ .
https://downloads.ibge.gov.br/downloads_...
-4747. Instituto Brasileiro de Geografia e Estatística (IBGE). Censo demográfico 2010 [Internet]. Brasil: IBGE ; 2010 [updated 2018]. Available from: Available from: http://www.ibge.gov.br/home/estatistica/ populacao/censo2010/default.shtm/ .
http://www.ibge.gov.br/home/estatistica/...
and the Secretariat for the Environment of the State of SP4848. Secretaria de Meio Ambiente do Estado de São Paulo (SMA). Rede de drenagem do estado de São Paulo obtida a partir da basedogisat (cartas topográficas na escala 1:50.000) por processo automático [Internet]. Coordenadoria de planejamento ambiental. São Paulo: SMA; 2013 [updated 2018]. Available from: Available from: http://www.ambiente.sp.gov.br/cpla/mapa-da-rede-de-drenagem-do-estado-de-sao-paulo/ .
http://www.ambiente.sp.gov.br/cpla/mapa-...
.

The data on autochthonous and imported cases and cases of unknown origin were analyzed for the periods 1978-1988, 1989-1999, 2000-2006, and 2007-2016. The first and second periods correspond to the time interval when reporting and investigation records were sent to SUCEN and organized manually. In the third and fourth periods, the data records were entered into the SINAN-W and SINAN-NET information systems, respectively. For the period 2000-2006, all cases were classified as those of unknown origin, probably due to the interruption of the epidemiological investigation of schistosomiasis in the region. The incidence rates of autochthonous and imported cases and those of unknown origin were calculated for municipalities with autochthonous occurrence of schistosomiasis according to the periods under consideration. The schistosomiasis cases were geocoded by home address using a batch geocoding tool4949. Zwiefelhofer D.B. Batch Geocoding [Internet]. Find Latitude and Longitude, 2008 [updated 2017]. Available from: Available from: http://www.findlatitudeandlongitude.com/batch-geocode/ .
http://www.findlatitudeandlongitude.com/...
, and the points corresponding to the geographical coordinates were imported in the format of latitude/longitude (datum WGS84) into the software QGIS version 2.145050. QGIS Development Team QGIS Version 2.14. Geographic Information System [Internet]. Open Source Geospatial Foundation Project; 2016 [updated 2018]. Available from: Available from: http://www.qgis.org/ .
http://www.qgis.org/...
.

For each of these municipalities with autochthonous occurrence and after the geocoding, the imported and autochthonous cases were computed according to census tracts and periods considered. This was accomplished through the complement MMQGIS5151. Minn M. MMQGIS. A collection of QGIS vector layer operation plugins. 2018 [updated 2018]. Available from: Available from: http://michaelminn.com/linux/mmqgis/ .
http://michaelminn.com/linux/mmqgis/...
in QGIS5050. QGIS Development Team QGIS Version 2.14. Geographic Information System [Internet]. Open Source Geospatial Foundation Project; 2016 [updated 2018]. Available from: Available from: http://www.qgis.org/ .
http://www.qgis.org/...
. The areas at greatest risk for schistosomiasis were identified using the spatial scan statistics in SaTScan version 9.45252. Kulldorff M. SaTScan-Software for the spatial, temporal, and space-time scan statistics [Internet]. Boston: Harvard Medical School and Harvard Pilgrim Health Care; 2015 [updated 2018]. Available from: Available from: http://www.satscan.org/ .
http://www.satscan.org/...
. For this, the populations in the middle of the period and centroid coordinates of the census tracts were also considered.

A spatial scan analysis was performed using the discrete Poisson model under the following conditions: maximum cluster size equal to 50% of the population and circular clusters5353. Kulldorff M. A spatial scan statistic. Commun Stat Theory Methods. 1997;26:1481-1496.-5454. Kulldorff M. SatScan Version 9.4. SaTScan Manual do Usuário. translator: Pellini ACG. Boston, MA, USA. Harvard Medical School and Harvard Pilgrim Health Care Institute. 2016. 113 p.. The analysis identified clusters where there was a high risk of occurrence of infection and associated relative risk (RR), which corresponds to the ratio of the incidence rate inside the cluster to the incidence rate outside it. The respective P-values were also calculated, and a P-value < 5% was considered statistically significant. In water bodies, overlapped high-risk clusters of autochthonous cases were identified in the spatial scan analysis of this study. In these peculiar water bodies, planorbids of the genus Biomphalaria were collected between 2015 and 2017, using a standard ladle recommended by the Brazilian Ministry of Health5555. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância e controle de moluscos de importância epidemiológica: diretrizes técnicas: Programa de Vigilância e Controle da Esquistossomose (PCE). 2th ed. Brasília: MS . 2008. 177 p.. The snails were identified by examination of the morphological characteristics of their reproductive apparatus as described in Paraense5656. Paraense WL, 1975. Estado atual da sistemática dos planorbídeos brasileiros. Arq Mus Nac.1975;55:105-128.-5757. Paraense WL. B. occidentalis sp. n. from South America. Mem Inst Oswaldo Cruz. 1981;76(2):199-211.. All snails were exposed to artificial light in the laboratory to induce shedding of trematode cercariae of Sm5555. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância e controle de moluscos de importância epidemiológica: diretrizes técnicas: Programa de Vigilância e Controle da Esquistossomose (PCE). 2th ed. Brasília: MS . 2008. 177 p..

The relationship between the spatial distribution of autochthonous and imported cases in the period 1978-2016 of the GeoSentinel sites in UGRHI-17 of Middle Paranapanema was analyzed using Ripley’s K12-function5858. Teixeira-Neto RG, Silva ES, Nascimento RA, Belo VS, Oliveira CDL, Pinheiro LC, et al. Canine visceral leishmaniasis in an urban setting of Southeastern Brazil: an ecological study involving spatial analysis. Parasit Vectors. 2014;7(1):485., in the R software version 3.2.25959. R Development Core Team version 3.2.2. R: A language and environment for statistical computing [Internet]. Vienna: R Foundation for Statistical Computing. 2015 [updated 2018]. Available from: Available from: https://cran.r-project.org/bin/windows/base/old/3.2.2/ .
https://cran.r-project.org/bin/windows/b...
with Splancs package6060. Bivand R, Rowlingson B, Diggle P, Petris G, Eglen S. Package ‘splancs’. R package version 2.01-40. 2017 [updated 2018]. Available from: Available from: https://cran.r-project.org/web/packages/splancs/splancs.pdf/ .
https://cran.r-project.org/web/packages/...
. This allowed the evaluation of the existence of spatial dependence between these two distributions and the radius of influence. The radius of influence data and geographical coordinates of the imported and autochthonous cases were subsequently used to estimate the kernel density to verify the lower and higher intensity probability of the occurrence of the cases in the geographical area. Red, green, and light blue colors were used to represent the areas where the densities of imported and autochthonous cases were mostly observed. This was achieved through Splancs package6060. Bivand R, Rowlingson B, Diggle P, Petris G, Eglen S. Package ‘splancs’. R package version 2.01-40. 2017 [updated 2018]. Available from: Available from: https://cran.r-project.org/web/packages/splancs/splancs.pdf/ .
https://cran.r-project.org/web/packages/...
in the R software5959. R Development Core Team version 3.2.2. R: A language and environment for statistical computing [Internet]. Vienna: R Foundation for Statistical Computing. 2015 [updated 2018]. Available from: Available from: https://cran.r-project.org/bin/windows/base/old/3.2.2/ .
https://cran.r-project.org/bin/windows/b...
.

Flow maps showing the origin of cases imported from other Brazilian states to the GeoSentinel sites and the internal flow of imported cases within the study area were obtained using information on PIS and the Flowmapper version 0.4.16161. Güllüoğlu C. FlowMapper v 0.4.1. [Internet]. QGIS Python Plugins Repository; 2016 [updated 2018]. Available from: Available from: https://plugins.qgis.org/plugins/FlowMapper/version/0.4.1/ .
https://plugins.qgis.org/plugins/FlowMap...
tool, an extension of QGIS5050. QGIS Development Team QGIS Version 2.14. Geographic Information System [Internet]. Open Source Geospatial Foundation Project; 2016 [updated 2018]. Available from: Available from: http://www.qgis.org/ .
http://www.qgis.org/...
.

RESULTS

In the period from 1978-2016, 4,085 schistosomiasis cases were noted in 25 municipalities (Table 1), 37.0% (1,511) of which were classified as autochthonous, 53.6% (2,189) as imported, and 9.4% (385) as being of unknown origin (i.e., cases that could not be classified because there was some uncertainty as to the municipality in which the infection had probably occurred or for which this information was not available).

During the study period, autochthonous cases were found in eight municipalities of this region (Table 1). Of these, 92.8% occurred in Ourinhos, 5.3% in Assis, and 0.9% in Ipaussu, totaling 99.0% of the total number of autochthonous cases. In the period 2000-2006, all cases were considered to be of unknown origin (Table 1, Figure 1). Throughout the entire period, 91.3% of the autochthonous cases were reported in urban areas.

Overall, there was a significant decrease in the number of schistosomiasis cases in the municipalities during the periods analyzed, with greater intensity in the three municipalities that have the greatest concentrations of autochthonous cases (Figure 1). Assis, Ipaussu, and São Pedro do Turvo only had autochthonous cases registered before the second study period (1989-1999), and Cândido Mota had autochthonous cases registered before the first period (1978-1988) (Table 1). However, it should be noted that only Ourinhos reported autochthonous cases before 2016 (three cases). The last autochthonous cases in Canitar, Chavantes, and Palmital were reported in 2008, 2009, and 2011, respectively. This decline was also observed in the number of imported cases and cases of unknown origin (Table 1). The last cases in both Ipaussu and Assis occurred in 2001 and 2008, respectively.

FIGURE 1:
Incidence rates of autochthonous, imported, and unknown origin cases of the eight municipalities with autochthony of the GeoSentinel sites of Middle Paranapanema, São Paulo, Brazil, according to the four study periods (1978-2016). Incidence rate per 1 million inhabitants per year. (Our, Ourinhos; Ipa, Ipaussu; CdM, Candido Mota; Pal, Palmital; Chv, Chavantes; Cnt, Canitar; SPT, São Pedro do Turvo) *Chv/Cnt = Canitar belonged to Chavantes until 1991 (state law nº 7644, of December 30, 1991).

High-risk clusters were only recognized in the spatial analysis of the SatScan in the census tracts of Ourinhos, Assis, and Ipaussu. In Ourinhos, in the first and second study periods, two clusters in which there was a high risk of autochthonous cases were identified. The first was associated with the Christoni stream, and the second with the Furninhas stream (Figure 2A1-2). In the period 2007-2016, a single cluster (RR=14.7) was found. Both streams lay within this cluster (Figure 2A3). Spatial clusters in Ourinhos were identified for imported cases in three of the periods studied (Figures 2A4-6). Comparison of the results of the cluster analysis shows the similarity between the clusters of autochthonous and imported cases, as well as their proximity to the Furninhas and Christoni streams.

FIGURE 2:
Maps of the municipalities of Ourinhos and Assis, São Paulo, Brazil, with spatial clusters of cases of schistosomiasis.

In the Christoni stream, the species B. glabrata and B. occidentalis were identified and in the Furninhas stream, B. occidentalis and B. tenagophila (Table 2). No snail eliminated cercariae of Sm.

TABLE 2:
Geographic coordinates and number of Biomphalaria Preston, 1910 species collected in water bodies in the municipality of Ourinhos, Assis, and Ipaussu, SP, Brazil, between 2015 and 2017.

In Assis, one high-risk cluster was found for the occurrence of autochthonous and imported cases in the period 1978-1988 and another in 1989-1999, near the Fortuninha and Jacu streams (Figure 2B1-4). The collection of snails in Assis to identify IH in clusters that were considered of high risk resulted in the following: B. glabrata was identified in the Fortuninha stream, while B. tenagophila and B. occidentalis were identified in the Jacu stream (Table 2).

In Ipaussu, a high-risk cluster was identified relating to the São Luiz stream, with autochthonous cases for the period 1989-1999 (RR=19.2), and another cluster with imported cases in the period 1978-1988 (RR=20.2). Both clusters were located in the urban areas. The São Luiz stream is currently colonized by B. tenagophila, B. occidentalis, and B. peregrina (Table 2).

Moreover, there was agreement between these clusters and the PIS identified in the databases. The PIS identified the greatest frequency of autochthonous cases in the following streams in Ourinhos: Christoni, in 43.4% (608); Furninhas, in 35.8% (503); Furnas, in 5.7% (80); and other water bodies (Turvo, Paranapanema, Pardo rivers and others), in 8.2% (115). However, in 6.8% (96) of the survey records, we observed a complete lack of information.

In Assis, there was agreement between PIS and cluster in the following water bodies: Jacu, in 35.0% (28); Fortuninha (Buracão park), in 20.0% (16); Aldeia stream, in 7.5% (6); and Canada farm lakes (Jacu neighborhood), in 5.0% (4). However, in 32.5% (26) of the records, no information was included. In Candido Mota, 50% (4) were identified in the Jacu stream (headwater in Assis6262. Bongiovanni S, Matos WH. Microbaciado córrego Jacu (Municípios de Assis e Cândido Mota, Oeste de São Paulo): Abordagem histórica, econômica e ambiental. [Internet]. Santa Catarina: Congresso Brasileiro de ciência e Tecnologia em Resíduos e desenvolvimento Sustentável; 2004;278-287 [updated 2018]. Available from: Available from: https://www.ipen.br/biblioteca/cd/ictr/2004/ARQUIVOS%20PDF/08/08-033.pdf/ .
https://www.ipen.br/biblioteca/cd/ictr/2...
), whereas others lacked any identification. In Ipaussu, a higher frequency of autochthonous cases was identified in the following water bodies: São Luiz stream, in 76.9% (10), Municipal lake, in 15.4% (2); and Paranapanema river reservoir, in 8% (1).

The graph of the K12-function analysis (Figure 3A) indicates the existence of positive spatial dependence to a distance of approximately 3,900 m between the imported and autochthonous cases, corroborated by the kernel density map analysis (Figure 3BC), where a higher concentration of cases may be seen in Ourinhos and Assis, for both autochthonous and imported cases.

FIGURE 3:
Graph of bivariate K12-function analysis (A). The blue curve that continues above the envelope shows a positive spatial dependence between imported and autochthonous cases of schistosomiasis, and Kernel density with radius of influence of ~ 3,900 m maps shows the distribution of imported (B) and autochthonous (C) cases in GeoSentinel sites of Middle Paranapanema, SP, Brazil.

Figure 4A shows the origin of cases imported from other Brazilian states for the GeoSentinel sites of Middle Paranapanema: Paraná (34.6%), Minas Gerais (16.8%), Alagoas (9.3%), Pernambuco (9.0%), Bahia (8.3%), and Sergipe (4.5%). Of the total number of imported cases, 27.0% belonged to the municipality of Ourinhos and 20.4% to Assis. In relation to the internal flow of cases of the study area, Ourinhos was the municipality that provided most imported cases to others (Figure 4B).

FIGURE 4:
Localization of GeoSentinel sites of Middle Paranapanema in the state of São Paulo, Brazil, South America; flow map of imported cases of schistosomiasis from other Brazilian states to the study area (A). Municipalities that compose the GeoSentinel sites; flow map with the internal flow of imported cases in the GeoSentinel sites (B) in the period 1978-2016.

DISCUSSION

The use of GIS and spatial analysis techniques in the study of schistosomiasis allowed us to specify in great detail, within the space occupied by the municipalities and their water bodies in the GeoSentinel sites of Middle Paranapanema, the areas with the highest risk for the transmission of schistosomiasis in different periods and map the origin of the imported cases. In delimiting risk areas, the GIS allows the orientation of the malacological surveillance to specific points, being fundamental tools for the improvement of the surveillance and control activities that may result in the elimination of schistosomiasis in the study region.

The results indicate a progressive decline in the incidence of schistosomiasis cases in the study region between 1978 and 2016. Only Ourinhos continued to be a significant area of autochthonous occurrence of the disease. In Cândido Mota, Assis, and Ipaussu, the last autochthonous cases of schistosomiasis occurred in the 1980s and 1990s. This reduction may be related to the process of urban development of the municipalities66. Katz N. Inquérito Nacional de Prevalência da Esquistossomose mansoni e Geo-helmintoses. Belo Horizonte: CPqRR; 2018. 76 p.,6363. Saiani CCS, Toneto Júnior R. Evolution of the access to services of basic sanitation in Brazil (1970 to 2004). Econom Soc. 2010;19(1):79-106.,6464. Fundação Sistema Estadual de Análise de Dados (SEADE). Informações dos municípios Paulistas. Portal de estatística do estado de São Paulo [Internet]. São Paulo: Fundação SEADE; 2016 [updated 2018]. Available from: Available from: http://www.imp.seade.gov.br .
http://www.imp.seade.gov.br...
and/or the appropriate treatment of patients3434. Organização Mundial de Saude (OMS). Trabalhando para superar o impacto global de doenças tropicais negligenciadas: Primeiro relatório da OMS sobre doenças tropicais negligenciadas. Brasília: OMS. 2010, 188 p.. It is important to bear in mind that the dynamics of the colonization and adaptation of IH species of Sm may affect the risk of disease transmission1919. Barbosa CS, Barbosa VS, Nascimento WC, Pieri OS, Araujo KCGM. Study of the snail intermediate hosts for Schistosoma mansoni on Itamaracá Island in northeast Brazil: spatial displacement of Biomphalaria glabrata by Biomphalaria straminea. Geospat Health. 2014;8:345-351..

The detection of the high-risk spatial cluster of schistosomiasis in the Christoni stream and the fact that this stream is still colonized by B. glabrata2727. Tuan R. Diversity and distribution of the Biomphalaria species in the middle reaches of the Paranapanema River, São Paulo, SP, Brazil. Biota Neotrop. 2009;9(1):279-283.,6565. Teles HMS. Ecological aspects of Biomphalaria Preston, 1910 in the State of Sao Paulo, Brazil. I. Syntopia. Cienc Cult. 1988;40(4):374-9.

66. Superintendência de Controle de Endemias (SUCEN). Boletim do Sistema de Vigilância Epidemiológico do ano de 1979-1980, do serviço Regional 11 - Marilia. Programa de Controle da Esquistossomose Mansônica no Estado de São Paulo, Secretaria de Estado da Saúde, SUCEN. 1980.
-6767. Superintendência de Controle de Endemias (SUCEN). Boletim do Sistema de Vigilância Epidemiológico do ano de 2009-2012, do serviço Regional 11 - Marilia. Programa de Controle da Esquistossomose Mansônica no Estado de São Paulo, Secretaria de Estado da Saúde, SUCEN. 2012., may characterize this stream as a transmission hotspot in Ourinhos. It is known that this IH species is best adapted to the development and propagation of the parasite2929. Magalhães LA, Dias LCS. Estudo da suscetibilidade da Biomphalaria glabrata de Ourinhos (SP), à infecção pelo Schistosoma mansoni de Belo Horizonte (MG), e de São José dos Campos (SP). Rev Saude Publica . 1973;7(3):295-7.,6868. Paraense WL. The schistosome vectors in the Americas. Mem Inst Oswaldo Cruz . 2001;96:7-16.. The flow map of imported cases demonstrates that Ourinhos is also an important nucleus for the regional dispersion of the disease.

The Christoni stream defines an area subject to flooding7070. Piroli VHB, Piroli EL. Deposição irregular de resíduos no leito das ruas de ourinhos e aumento das enxurradas e inundações. Periódico Eletrônico Fórum Ambiental da Alta Paulista. 2015;11(6):16-27., with vegetable gardens in meadows7171. Laurenti AEM, Piroli EL. Evolução do uso e ocupação do solo sobre as áreas de preservação permanente da microbacia urbana do córrego Christone 1972-2006 Ourinhos-SP. Rev Tópos. 2011;5(1):87-102. that seem to constitute an ideal ecosystem for the breeding of B. glabrata, which allows us to hypothesize that this stream is an important site for the transmission of the species and, consequently, the disease.

In addition to the Christoni stream, a high-risk cluster was identified in the Furninhas stream in Ourinhos, previously colonized by B. glabrata2727. Tuan R. Diversity and distribution of the Biomphalaria species in the middle reaches of the Paranapanema River, São Paulo, SP, Brazil. Biota Neotrop. 2009;9(1):279-283.,6666. Superintendência de Controle de Endemias (SUCEN). Boletim do Sistema de Vigilância Epidemiológico do ano de 1979-1980, do serviço Regional 11 - Marilia. Programa de Controle da Esquistossomose Mansônica no Estado de São Paulo, Secretaria de Estado da Saúde, SUCEN. 1980. but currently by B. tenagophila. The Furninhas stream has recently been the target of a significant intervention, not only along the urban stretch of the stream (reduction in tree coverage and canalization) but also in the rural stretch (replacement of pasture and annual crops by sugarcane plantations)7272. Piroli EL, Ishikawa DTK, Demarchi JC. Análise das mudanças no uso do solo da microbacia do córrego das Furnas, município de Ourinhos-SP, entre os anos de 1972 e 2007, e dos impactos sobre suas áreas de preservação permanente, apoiada em geoprocessamento. Curitiba, Brasil: Simpósio Brasileiro de Sensoriamento Remoto, INPE; 2011;(15):6333-6340., favoring the substitution of native species by B. tenagophila. This hypothesis might explain the decrease in the number of cases observed in this municipality. B. tenagophila has reproductive and physiological characteristics that enable it to proliferate in modified environments7373. Guimarães MCDA, Menezes RMTD, Tuan R. Experimental study on reproduction of the freshwater snail Biomphalaria tenagophila (d’Orbigny, 1835). Invertebr Reprod Dev. 2016;60(2):145-51. and has a limited capacity to act as an IH of Sm7474. Paraense WL, Côrrea LR. Differential susceptibility of Biomphalaria tenagophila populations to infection with a strain of Schistosoma mansoni. J Parasitol. 1978;64:822-6.,7575. Guaraldo AMA, Magalhães LA, Rangel HDA, Pareja G. The evolution of sporocysts of Schistosoma mansoni, Sambon, 1907, in Biomphalaria glabrata (Say, 1818) and in Biomphalaria tenagophila (D'Orbigny, 1835). Rev Saude Publica . 1981;15(4):436-48..

In Ourinhos, there are still areas where there is no piped wastewater system and some of the sewage is disposed of untreated. According to the National Sanitation Information System data, 78.6% of the water consumed by the municipality in 2015 was collected as sewage, and only 68.0% of this was treated7676. Secretaria Nacional de Saneamento Ambiental (SNSA). Sistema Nacional de Informações sobre Saneamento. SNIS - Série Histórica [Internet]. Brasilia: Ministério das Cidades, SNSA;. 2015 [updated 2017; cited 2018]. Available from: Available from: http://app.cidades.gov.br/serieHistorica/ .
http://app.cidades.gov.br/serieHistorica...
. Sewage that is neither collected nor treated can contaminate watercourses as it may contain feces from infected individuals, allowing the disease cycle to be completed when IHs are present5555. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância e controle de moluscos de importância epidemiológica: diretrizes técnicas: Programa de Vigilância e Controle da Esquistossomose (PCE). 2th ed. Brasília: MS . 2008. 177 p.. In Ourinhos, as many of these water bodies are near residential areas, they can be readily accessed by the local community, leading to the continued occurrence of infection6969. Figueiredo WSA, Epidemiologia da esquistossomose mansônica e o processo de organização espacial: o caso do município de Ourinhos, São Paulo. [São Paulo]: Faculdade de Saúde Pública-USP. Departamento de Epidemiologia. 2000: 40-52, 127-137 p.. Our results corroborate the findings of other authors6565. Teles HMS. Ecological aspects of Biomphalaria Preston, 1910 in the State of Sao Paulo, Brazil. I. Syntopia. Cienc Cult. 1988;40(4):374-9.,8585. Silva LJ. Crescimento urbano e doença: a esquistossomose no município de São Paulo (Brasil). Rev Saude Publica . 1985;19(1):1-7.,8686. Coura-Filho P. Schistosomiasis mansoni in urban territory. 2. A theoretical approach to the accumulation, concentration, and centralization of capital and the production of disease. Cad Saude Publica . 1997;13(3):415-24. who have shown that most infection sites were close to dwellings, i.e., transmission was peri-domiciliary.

In Assis, between 1978 and 1999, clusters were found around the Fortuninha and the Jacú streams. In contrast with Ourinhos, in Assis, the sanitation has recently improved, and in 2015, 83.7% of the volume of water consumed was collected as sewage and treated7676. Secretaria Nacional de Saneamento Ambiental (SNSA). Sistema Nacional de Informações sobre Saneamento. SNIS - Série Histórica [Internet]. Brasilia: Ministério das Cidades, SNSA;. 2015 [updated 2017; cited 2018]. Available from: Available from: http://app.cidades.gov.br/serieHistorica/ .
http://app.cidades.gov.br/serieHistorica...
. The increased coverage of sewage collection and water treatment may explain the elimination of the disease in the city. Other authors have also correlated the sewage collection coverage with the decrease in the number of cases of this disease and other intestinal parasite diseases in Assis7777. Ludwig KM, Frei F, Alvares Filho F, Ribeiro-Paes JT. Correlation between sanitation conditions and enteroparasitoses in the population of Assis, Sao Paulo State, Brazil. Rev Soc Bras Med Trop . 1999;32(5):547-55.,7878. Frei F, Juncansen C, Ribeiro-Paes JT. Epidemiological survey of intestinal parasite infections: analytical bias due to prophylactic treatment. Cad Saude Publica . 2008;24(12):2919-25., demonstrating the impact of basic sanitation on intestinal infectious diseases66. Katz N. Inquérito Nacional de Prevalência da Esquistossomose mansoni e Geo-helmintoses. Belo Horizonte: CPqRR; 2018. 76 p.,7979. Teixeira JC, Oliveira GSD, Viali ADM, Muniz SS. Study of the impact of deficiencies of sanitation on public health in Brazil from 2001 to 2009. Eng Sanit Ambient. 2014;19(1):87-96.. Although the Fortuninha stream is still colonized by B. glabrata6666. Superintendência de Controle de Endemias (SUCEN). Boletim do Sistema de Vigilância Epidemiológico do ano de 1979-1980, do serviço Regional 11 - Marilia. Programa de Controle da Esquistossomose Mansônica no Estado de São Paulo, Secretaria de Estado da Saúde, SUCEN. 1980.,8080. Perez MD, Santos MR, Ishihata JK. Contribution to the survey of the Planorbis map in the State of São Paulo; investigation of centres of Schistosoma mansoni infection in its evolutionary form.III. Hydrographic area of Assis-Cândido Mota (Paranapanema Valley). Hospital, Rio de Janeiro. 1968;74:495-507., it has been channeled, and lakes have been constructed, making it a public park8181. Menarin CA. Leituras do espaço e da política: elementos para uma história ambiental urbana. II colóquio da pós-graduação em letras “Literatura e Vida Social” UNESP, 2010: 267-282.. The same has happened to the Jacu stream, that has undergone changes in width and depth, recomposition of the gallery forest8282. Brússolo RG, Ely DF. O clima e a cidade: Ilhas de calor em Assis/SP. Formação, 2015;2(22):99-127., and channeling in its urban stretch8383. Rodrigues ACJ, Palmieri DA, Rodrigues RJ. Uso do geoprocessamento para planejamento, manejo e proteção de mananciais em áreas urbanas. Tekhne e Logos. 2018;9(1): 53-67., conditions that must have favored the replacement of B. glabrata6666. Superintendência de Controle de Endemias (SUCEN). Boletim do Sistema de Vigilância Epidemiológico do ano de 1979-1980, do serviço Regional 11 - Marilia. Programa de Controle da Esquistossomose Mansônica no Estado de São Paulo, Secretaria de Estado da Saúde, SUCEN. 1980.,8080. Perez MD, Santos MR, Ishihata JK. Contribution to the survey of the Planorbis map in the State of São Paulo; investigation of centres of Schistosoma mansoni infection in its evolutionary form.III. Hydrographic area of Assis-Cândido Mota (Paranapanema Valley). Hospital, Rio de Janeiro. 1968;74:495-507.by B. tenagophila and B. occidentalis.

Another example of the influence of anthropic alterations on the transmission dynamics of schistosomiasis is found in the observation, in Ipaussu, of the limitation of schistosomiasis to the first two periods analyzed in this study. This coincides with the colonization of the main stream of Ipaussu (São Luiz) by B. glabrata6666. Superintendência de Controle de Endemias (SUCEN). Boletim do Sistema de Vigilância Epidemiológico do ano de 1979-1980, do serviço Regional 11 - Marilia. Programa de Controle da Esquistossomose Mansônica no Estado de São Paulo, Secretaria de Estado da Saúde, SUCEN. 1980., sometimes found infected with Sm3131. Piza JDT, Ramos ADS, 1960. Os focos autóctones de esquistossomose no Estado de São Paulo. Arq Hig Saude Publica. 25(86):261-71.,6666. Superintendência de Controle de Endemias (SUCEN). Boletim do Sistema de Vigilância Epidemiológico do ano de 1979-1980, do serviço Regional 11 - Marilia. Programa de Controle da Esquistossomose Mansônica no Estado de São Paulo, Secretaria de Estado da Saúde, SUCEN. 1980.. Currently, the levels of fecal coliforms in the São Luiz stream are within the levels allowed by law8484. Borda AA, Branco JR AC. Perfil físico-químico, microbiológico e ecológico de mananciais dágua na área urbana do município de Ipaussu, São Paulo. Salvador/BA IV: Congresso Brasileiro de Gestão Ambiental. 2013:1-9., indicating that there has been a significant improvement in freshwater quality, which in theory may have favored the replacement of B. glabrata by B. tenagophila, as has been observed since 20032727. Tuan R. Diversity and distribution of the Biomphalaria species in the middle reaches of the Paranapanema River, São Paulo, SP, Brazil. Biota Neotrop. 2009;9(1):279-283.,6767. Superintendência de Controle de Endemias (SUCEN). Boletim do Sistema de Vigilância Epidemiológico do ano de 2009-2012, do serviço Regional 11 - Marilia. Programa de Controle da Esquistossomose Mansônica no Estado de São Paulo, Secretaria de Estado da Saúde, SUCEN. 2012., resulting in a reduction in the risk of the transmission of schistosomiasis.

The results of the scan statistics show that the clusters of imported cases coincide with the clusters of autochthonous cases in Ourinhos, Assis, and Ipaussu. These areas had already been identified by Figueiredo6969. Figueiredo WSA, Epidemiologia da esquistossomose mansônica e o processo de organização espacial: o caso do município de Ourinhos, São Paulo. [São Paulo]: Faculdade de Saúde Pública-USP. Departamento de Epidemiologia. 2000: 40-52, 127-137 p. as having significant numbers of autochthonous cases and therefore qualifying for consideration as important potential transmission areas. This result is consistent with that obtained by Ripley’s K12-function, which showed that there is a positive spatial dependence between autochthonous and imported cases, with the result that both the addresses of the imported and autochthonous cases provide important information about the transmission sites.

The vast majority of cases imported into the study region came from Paraná and Minas Gerais states. The municipality of Jacarezinho in Paraná, which borders Ourinhos, has been a focus of schistosomiasis since 19488787. Coutinho JO, Pessôa SB. Sobre um foco autóctone da Esquistossomose mansonica em Jacarezinho (Norte do Paraná). Hospital, Rio de Janeiro. 1948;31(4):531-42. and has the presence of B. glabrata8888. Luz E, Silva SM, Carvalho AP, Castro N. Atualização da sistemática e de planorbídeos (Gasteropoda, Pulmonata) no Estado do Paraná (Brasil). Acta Biológica Paranaense. 1998;27. and B. tenagophila5555. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância e controle de moluscos de importância epidemiológica: diretrizes técnicas: Programa de Vigilância e Controle da Esquistossomose (PCE). 2th ed. Brasília: MS . 2008. 177 p.,8989. Costa AB, Bravo DS, Guilherme TS, Marqui R, Silva FTR, Melo SCCS. Esquistossomose Urbana no Norte Pioneiro do Estado do Paraná, Brasil. J Health Sci, 2017;19(4):251-5.. The presence of an economic pole in Ourinhos may be a determining factor accounting for the human migratory flow from northern Paraná. The migratory movement from Minas Gerais merits the attention of epidemiological research services because this state has highly endemic areas for schistosomiasis related to B. glabrata55. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: diretrizes técnicas. 4a edição. Brasília: MS; 2014. 13-20 p.,3030. Chieffi PP, Waldman EA. Aspectos particulares do comportamento epidemiológico da esquistossomose mansônica no Estado de São Paulo, Brasil. Cad Saude Publica . 1988;4(3):257-75.,8585. Silva LJ. Crescimento urbano e doença: a esquistossomose no município de São Paulo (Brasil). Rev Saude Publica . 1985;19(1):1-7.,9090. Souza CPD, Caldeira RL, Drummond SC, Melo AL, Guimarães CT, Soares DDM, et al. Geographical distribution of Biomphalaria snails in the state of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz . 2001;96(3):293-302.. Possibly, this disease was introduced in SP, just as in Paraná, by infected immigrants from Minas Gerais and the Northeastern region of the country8585. Silva LJ. Crescimento urbano e doença: a esquistossomose no município de São Paulo (Brasil). Rev Saude Publica . 1985;19(1):1-7..

The limitations of this study are its use of secondary data on the occurrence of schistosomiasis underlying which are two important components: failures in the classification of cases and identification of the respective PIS and the underreporting of cases. If we consider that, according to Eduardo et al.9191. Eduardo MBP, Souza D, Ciaravolo RMC, Kanamura HY, Gargioni C, Falcão ACMG. Esquistossomose mansônica no Estado de São Paulo. Aspectos epidemiológicos. Bol Epidem Paul. 2005;18:2-8., 30% of cases of unknown origin should in fact be classified as autochthonous, it follows that the schistosomiasis in the study area has been underestimated. This problem had already been noted by Bezerra9292. Bezerra IA. Situação da notificação em esquistossomose na Grande São Paulo (Brasil), no período de 1982 a 1983. Rev Saude Publica . 1984;18(5):386-95., who stressed the importance of training staff to reduce the number of mistakes in the reporting and investigation of the records relating to the disease.

The failure to undertake surveillance and control of schistosomiasis may be associated with the decentralization of these actions that was officially sanctioned in 199955. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: diretrizes técnicas. 4a edição. Brasília: MS; 2014. 13-20 p.,9393. Ministério da Saude (MS), Portaria no1.399, de 15 de dezembro de 1999. Regulamenta a NOB SUS 01/96 no que se refere às competências da União, Estados, Municípios e Distrito Federal, na área de epidemiologia e controle de doenças, define a sistemática de financiamento. Brasília: MS , Diário Oficial da União; 1999, Seção 1.. From that year on, reporting became the responsibility of the municipalities, and many cases ceased to be classified or investigated. The problem was solved in 2003, with the resumption of schistosomiasis surveillance and control activities55. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: diretrizes técnicas. 4a edição. Brasília: MS; 2014. 13-20 p.,9494. Barbosa CS, Silva CBD, Barbosa FS. Esquistossomose: reprodução e expansão da endemia no Estado de Pernambuco no Brasil. Rev Saude Publica . 1996;609-16.

95. Wanderley DMV, Glasser CM, Silva B, Teles FB, 2006. Superintendência de Controle de Endemias-Sucen: 30 anos de trajetória. Suplemento especial, Bol Epidem Paul . 2006;3-9.
-9696. Centro de vigilância epidemiológica “prof. Alexandre Vranjac”. Vigilância epidemiológica e controle da esquistossomose: normas e instruções. São Paulo: CVE . 2007, 45 p.. Underreporting contributes to the characterization of schistosomiasis as a neglected tropical disease, which is not accorded priority by public health policies3434. Organização Mundial de Saude (OMS). Trabalhando para superar o impacto global de doenças tropicais negligenciadas: Primeiro relatório da OMS sobre doenças tropicais negligenciadas. Brasília: OMS. 2010, 188 p.,9797. Tibiriçá SHC, Guimarães FB, Teixeira MTB. A esquistossomose mansoni no contexto da política de saúde brasileira. Cien Saude Colet . 2011;16:1375-81.,9898. Araujo ISD, Moreira ADL, Aguiar R. Doenças negligenciadas, comunicação negligenciada. Apontamentos para uma pauta política e de pesquisa. Rev Eletron Comun Inf Inov Saude. Rio de Janeiro. 2013;6(4)..

In contrast, the strength of this study is the association of geoprocessing techniques with epidemiological studies so that the objectives of the study could be achieved. Moreover, these tools are useful for the elaboration of strategies of action and have the potential to improve the system of surveillance and control of schistosomiasis.

Finally, this study shows that there has been a general decrease in the incidence of schistosomiasis in the GeoSentinel sites, in UGRHI-17 of Middle Paranapanema. In Ourinhos, schistosomiasis persists but has low incidence, though it still represents a public health problem. In this municipality, the health services should invest in the early detection of the disease, adequate notification and classification of autochthonous cases, malacological surveillance of the water bodies containing B. glabrata, and improvements in basic sanitation. These are measures that would make the elimination of schistosomiasis on the short term conceivable with a resulting impact throughout the region.

Ethical Approval

The project was approved by the School of Public Health Committee for Ethics in Research (COEP) of USP. Approval was granted through the Plataforma Brasil system (Ministry of Health, National Health Council) under reference number 53559816.0.0000.5421.

ACKNOWLEDGMENTS

The authors would like to thank the Superintendence for the Control of Endemic Diseases (SUCEN) and Alexandre Vranjak Center for Epidemiological Surveillance (CVE) for providing information.

REFERENCES

  • 1
    Rollemberg CVV, Santos CMB, Silva MMBL, Souza AMB, Silva ÂM, Almeida JAP, et al. Aspectos epidemiológicos e distribuição geográfica da esquistossomose e geo-helmintos, no Estado de Sergipe, de acordo com os dados do Programa de Controle da Esquistossomose. Rev Soc Bras Med Trop. 2011;44(1):91-96.
  • 2
    Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. The Lancet 2014;383(9936);2253-2264.
  • 3
    World Health Organization (WHO). Schistosomiasis and soil-transmitted helminthiases: number of people treated in 2016. Weekly Epidemiological Record: WHO; 2017. 92(49):749-760 p.
  • 4
    World Health Organization (WHO). Schistosomiasis: status of schistosomiasis endemic countries: 2017. WHO; 2018 [updated 2018]. Available from: http://www.who.int/neglected_diseases/ntddata/sch/sch.html
    » http://www.who.int/neglected_diseases/ntddata/sch/sch.html
  • 5
    Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: diretrizes técnicas. 4a edição. Brasília: MS; 2014. 13-20 p.
  • 6
    Katz N. Inquérito Nacional de Prevalência da Esquistossomose mansoni e Geo-helmintoses. Belo Horizonte: CPqRR; 2018. 76 p.
  • 7
    Medronho RDA. Geoprocessamento e saúde: uma nova abordagem do espaço no processo saúde doença. Rio de Janeiro: FIOCRUZ/CICT/NECT; 1995.
  • 8
    Vine MF, Degnan D, Hanchette C. Geographic Information Systems: Their use in environmental epidemiologic research. Environ Health Perspect. 1997;105:598-605.
  • 9
    Organización Panamericana de la Salud (OPS). Uso de los Sistemas de Información Geográfica en Epidemiología (SIG-EPI), Bol Epidemiol. 1996;17(1):1-6.
  • 10
    Carvalho MS, Pina MF, Santos SM. Conceitos Básicos de Sistemas de Informação Geográfica e Cartografia Aplicados à Saúde. Brasília. Organização Panamericana de Saúde, Ministério da Saúde. 2000; 124 p.
  • 11
    Carvalho MS, Souza-Santos R. Analysis of spatial data in public health: methods, problems, and perspectives. Cad Saude Publica. 2005;21(2):361-78.
  • 12
    Austin MP. Spatial prediction of species distribution: an interface between ecological theory and statistical modelling. Ecological modelling. 2002;157(2):101-18.
  • 13
    Waller LA, Gotway CA. Applied Spatial Statistics for Public Health Data. New Jersey: John Wiley & Sons; 2004. 520 p.
  • 14
    Bavia ME, Hale LF, Malone JB, Braud DH, Shane SM. Geographic information systems and the environmental risk of schistosomiasis in Bahia, Brazil. Am J Trop Med Hyg. 1999;60(4):566-72.
  • 15
    Cardim LL, Ferraudo AS, Pacheco STA, Reis RB, Silva MMN, Carneiro DDMT, et al. Análises espaciais na identificação das áreas de risco para a esquistossomose mansônica no município de Lauro de Freitas, Bahia, Brasil. Cad Saude Publica . 2011;899-908.
  • 16
    Gomes E, Leal-Neto OB, Albuquerque J, da Silva H, Barbosa CS. Schistosomiasis transmission and environmental change: a spatio-temporal analysis in Porto de Galinhas, Pernambuco-Brazil. Int J Health Geogr. 2012;11(1):51.
  • 17
    Guimarães RJ, Fonseca FR, Dutra LV, Freitas CC, Oliveira GC, Carvalho OS. A study of Schistosomiasis prevalence and risk of snail presence spatial distributions using geo-statistical tools. In Schistosomiasis. Prof Mohammad Bagher Rokni (Ed.) InTech. 2012;255-80.
  • 18
    Fonseca F, Freitas C, Dutra L, Guimarães R, Carvalho O. Spatial modeling of the Schistosomiasis mansoni in Minas Gerais State, Brazil using spatial regression. Acta Trop. 2014;133:56-63.
  • 19
    Barbosa CS, Barbosa VS, Nascimento WC, Pieri OS, Araujo KCGM. Study of the snail intermediate hosts for Schistosoma mansoni on Itamaracá Island in northeast Brazil: spatial displacement of Biomphalaria glabrata by Biomphalaria straminea Geospat Health. 2014;8:345-351.
  • 20
    Santos ADD, Lima ACR, Santos MB, Alves JAB, Góes MADO, Nunes MAP, et al. Spatial analysis for the identification of risk areas for schistosomiasis mansoni in the State of Sergipe, Brazil, 2005-2014. Rev Soc Bras Med Trop . 2016;49(5):608-15.
  • 21
    Anaruma-Filho F, Sant'Ana JM, dos Santos RF, Castagna CL. Environmental inducers of Schistosomiasis mansoni in Campinas, Brazil. Geospat Health . 2010;5(1):79-91.
  • 22
    Teles HMS, Ferreira CS, Carvalho MED. Assessment of control and epidemiologic details of the schistosomiasis mansoni in Bananal, São Paulo, Brazil. Rev Bras Epidemiol. 2014;17:531-42.
  • 23
    Ferreira JM, Meira JA. Três casos de esquistossomose mansoni procedentes do interior do Estado de São Paulo (Ourinhos, Palmital e Ipauçu). Foco autóctone na cidade de Ourinhos. Rev Paul Med. 1952;41(1):15-8.
  • 24
    Piza JDT, Ramos ADS, Moraes LDC, Corrêa RDR, Takaku L, Pinto ADM. Carta planorbídica do Estado de São Paulo. Secretaria de Estado da Saúde, Campanha de Combate à Esquistossomose (CACEsq) São Paulo, 1972.
  • 25
    Teles HMS, Vaz JF. Distribuição de Biomphalaria glabrata (Say, 1818) (Pulmonata, Planorbidae) no estado de São Paulo, Brasil. Rev Saude Publica. 1987;21(6):508-12.
  • 26
    Teles HMS. Distribuição geográfica das espécies dos caramujos transmissores de Schistosoma mansoni no Estado de São Paulo. Rev Soc Bras Med Trop . 2005;38(5):426-32.
  • 27
    Tuan R. Diversity and distribution of the Biomphalaria species in the middle reaches of the Paranapanema River, São Paulo, SP, Brazil. Biota Neotrop. 2009;9(1):279-283.
  • 28
    Rey L. Primeiro encontro de planorbídeos naturalmente infestados por furcocercárias de S. mansoni no planalto paulista (Ourinhos). Rev Clín Sao Paulo. 1952;28:57-64.
  • 29
    Magalhães LA, Dias LCS. Estudo da suscetibilidade da Biomphalaria glabrata de Ourinhos (SP), à infecção pelo Schistosoma mansoni de Belo Horizonte (MG), e de São José dos Campos (SP). Rev Saude Publica . 1973;7(3):295-7.
  • 30
    Chieffi PP, Waldman EA. Aspectos particulares do comportamento epidemiológico da esquistossomose mansônica no Estado de São Paulo, Brasil. Cad Saude Publica . 1988;4(3):257-75.
  • 31
    Piza JDT, Ramos ADS, 1960. Os focos autóctones de esquistossomose no Estado de São Paulo. Arq Hig Saude Publica. 25(86):261-71.
  • 32
    Waldman EA, Silva LJ, Monteiro CA. Trajetória das Doenças Infecciosas: da Eliminação da Poliomielite à Reintrodução da Cólera. Inf Epidemiol Sus. 1999;8(3):5-47.
  • 33
    Barata RB. Cem anos de endemias e epidemias. Cien Saude Colet. 2000;5(2):333-45.
  • 34
    Organização Mundial de Saude (OMS). Trabalhando para superar o impacto global de doenças tropicais negligenciadas: Primeiro relatório da OMS sobre doenças tropicais negligenciadas. Brasília: OMS. 2010, 188 p.
  • 35
    World Health Organization (WHO). Schistosomiasis: progress report 2001-2011 and strategic plan 2012-2020. Geneva: WHO; 2013, 74 p.
  • 36
    Comitê da Bacia Hidrográfica do Médio Paranapanema (CBH-MP). Relatório de Situação dos Recursos Hídricos 2018 (Ano Base: 2017) - UGRHI-17. CBH-MP. 2018. [updated 2019]. Available from: Available from: http://cbhmp.org/publicacoes/relatorios/
    » http://cbhmp.org/publicacoes/relatorios/
  • 37
    Comitê da Bacia Hidrográfica do Médio Paranapanema (CBH-MP). Relatório Zero Relatório de Situação dos Recursos Hídricos da UGRHI-17 | ano: 1999. CBH-MP, 1999. [updated 2019]. Available from: Available from: http://cbhmp.org/publicacoes/relatorioz/
    » http://cbhmp.org/publicacoes/relatorioz/
  • 38
    Eduardo MBP. Avaliação da Esquistossomose no Estado de São Paulo. Documento técnico/Relatório de Avaliação. Secretaria do Estado da Saúde, Coordenadoria de Controle de Doenças, Centro de Vigilância Epidemiológica, Divisão de Doenças de Transmissão Hídrica e Alimenta, 2008, 59 p.
  • 39
    Instituto Brasileiro de Geografia e Estatística (IBGE). Estimativas de população residente nos Municípios Brasileiros com data de referência em 1º de julho de 2018. IBGE; 2018 [updated 2019]. Available from: Available from: https://www.ibge.gov.br/estatisticas-novoportal/sociais/populacao/9103-estimativas-de-populacao.html?=&t=resultados/
    » https://www.ibge.gov.br/estatisticas-novoportal/sociais/populacao/9103-estimativas-de-populacao.html?=&t=resultados/
  • 40
    Sistema de Informação de Agravos de Notificação (SINAN). Casos confirmados por Evolução e por Autóctone Mun. Res. segundo UF Notificação [Internet]. Brasília: SINAN Net. Ministério da Saúde/SVS; 2018 [updated 2018]. Available from: Available from: http://portalsinan.saude.gov.br/sinan-net/
    » http://portalsinan.saude.gov.br/sinan-net/
  • 41
    Centro de Vigilância Epidemiológica (CVE). Vigilância Epidemiológica. Divisão de Doenças de Transmissão Hídrica e Alimentar. Esquistossomose - [Dados estatísticos 1981 - 2009 - definitivo] [Internet]. São Paulo: CVE; 2011 [updated 2018]. Available from: Available from: http://www.cve.saude.sp.gov.br/
    » http://www.cve.saude.sp.gov.br/
  • 42
    Peron AF, Piroli EL. Projeto APPs: Conhecendo e cuidando da bacia hidrográfica do Rio Pardo. CEDIAP-GEO- Centro de Estudo e Divulgação de Informações sobre Áreas Protegidas, Bacias Hidrográficas e Geoprocessamento 1th ed. 2011. 23 p.
  • 43
    Instituto Brasileiro de Geografia e Estatística (IBGE). Anuário estatístico do Brasil 1982 [Internet]. Rio de Janeiro: IBGE; 1983 [updated 2018]. Available from:Available from:http://seculoxx.ibge.gov.br/images/seculoxx/arquivos_download/populacao/1982/populacao_m_1982aeb_016_a_017.xls/
    » http://seculoxx.ibge.gov.br/images/seculoxx/arquivos_download/populacao/1982/populacao_m_1982aeb_016_a_017.xls/
  • 44
    Instituto Brasileiro de Geografia e Estatística (IBGE). Setor Censitário 2010. Mapas, bases e referenciais, bases cartográficas, malhas digitais, Instituto Brasileiro de Geografia e Estatística [Internet]. Brasil: IBGE; 2010 [updated 2018]. Available from: Available from: http://mapas.ibge.gov.br/
    » http://mapas.ibge.gov.br/
  • 45
    Instituto Brasileiro de Geografia e Estatística (IBGE). Base Contínua 250 mil, Hidrografia. Mapas, Interativos, serviços, serviços do ArcGIS [Internet]. Brasil: IBGE ; 2010 [updated 2018]. Available from: Available from: http://mapas.ibge.gov.br/
    » http://mapas.ibge.gov.br/
  • 46
    Instituto Brasileiro de Geografia e Estatística (IBGE). Estimativas populacionais para os municípios e para as Unidades da Federação brasileiros em 01.07.1994 [Internet]. Brasil: IBGE ; 2016 [updated 2018]. Available from: Available from: https://downloads.ibge.gov.br/downloads_estatisticas.htm? Caminho=/Estimativas_de_ Populacao/Estimativas_1994/
    » https://downloads.ibge.gov.br/downloads_estatisticas.htm? Caminho=/Estimativas_de_ Populacao/Estimativas_1994/
  • 47
    Instituto Brasileiro de Geografia e Estatística (IBGE). Censo demográfico 2010 [Internet]. Brasil: IBGE ; 2010 [updated 2018]. Available from: Available from: http://www.ibge.gov.br/home/estatistica/ populacao/censo2010/default.shtm/
    » http://www.ibge.gov.br/home/estatistica/ populacao/censo2010/default.shtm/
  • 48
    Secretaria de Meio Ambiente do Estado de São Paulo (SMA). Rede de drenagem do estado de São Paulo obtida a partir da basedogisat (cartas topográficas na escala 1:50.000) por processo automático [Internet]. Coordenadoria de planejamento ambiental. São Paulo: SMA; 2013 [updated 2018]. Available from: Available from: http://www.ambiente.sp.gov.br/cpla/mapa-da-rede-de-drenagem-do-estado-de-sao-paulo/
    » http://www.ambiente.sp.gov.br/cpla/mapa-da-rede-de-drenagem-do-estado-de-sao-paulo/
  • 49
    Zwiefelhofer D.B. Batch Geocoding [Internet]. Find Latitude and Longitude, 2008 [updated 2017]. Available from: Available from: http://www.findlatitudeandlongitude.com/batch-geocode/
    » http://www.findlatitudeandlongitude.com/batch-geocode/
  • 50
    QGIS Development Team QGIS Version 2.14. Geographic Information System [Internet]. Open Source Geospatial Foundation Project; 2016 [updated 2018]. Available from: Available from: http://www.qgis.org/
    » http://www.qgis.org/
  • 51
    Minn M. MMQGIS. A collection of QGIS vector layer operation plugins. 2018 [updated 2018]. Available from: Available from: http://michaelminn.com/linux/mmqgis/
    » http://michaelminn.com/linux/mmqgis/
  • 52
    Kulldorff M. SaTScan-Software for the spatial, temporal, and space-time scan statistics [Internet]. Boston: Harvard Medical School and Harvard Pilgrim Health Care; 2015 [updated 2018]. Available from: Available from: http://www.satscan.org/
    » http://www.satscan.org/
  • 53
    Kulldorff M. A spatial scan statistic. Commun Stat Theory Methods. 1997;26:1481-1496.
  • 54
    Kulldorff M. SatScan Version 9.4. SaTScan Manual do Usuário. translator: Pellini ACG. Boston, MA, USA. Harvard Medical School and Harvard Pilgrim Health Care Institute. 2016. 113 p.
  • 55
    Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância e controle de moluscos de importância epidemiológica: diretrizes técnicas: Programa de Vigilância e Controle da Esquistossomose (PCE). 2th ed. Brasília: MS . 2008. 177 p.
  • 56
    Paraense WL, 1975. Estado atual da sistemática dos planorbídeos brasileiros. Arq Mus Nac.1975;55:105-128.
  • 57
    Paraense WL. B. occidentalis sp. n. from South America. Mem Inst Oswaldo Cruz. 1981;76(2):199-211.
  • 58
    Teixeira-Neto RG, Silva ES, Nascimento RA, Belo VS, Oliveira CDL, Pinheiro LC, et al. Canine visceral leishmaniasis in an urban setting of Southeastern Brazil: an ecological study involving spatial analysis. Parasit Vectors. 2014;7(1):485.
  • 59
    R Development Core Team version 3.2.2. R: A language and environment for statistical computing [Internet]. Vienna: R Foundation for Statistical Computing. 2015 [updated 2018]. Available from: Available from: https://cran.r-project.org/bin/windows/base/old/3.2.2/
    » https://cran.r-project.org/bin/windows/base/old/3.2.2/
  • 60
    Bivand R, Rowlingson B, Diggle P, Petris G, Eglen S. Package ‘splancs’. R package version 2.01-40. 2017 [updated 2018]. Available from: Available from: https://cran.r-project.org/web/packages/splancs/splancs.pdf/
    » https://cran.r-project.org/web/packages/splancs/splancs.pdf/
  • 61
    Güllüoğlu C. FlowMapper v 0.4.1. [Internet]. QGIS Python Plugins Repository; 2016 [updated 2018]. Available from: Available from: https://plugins.qgis.org/plugins/FlowMapper/version/0.4.1/
    » https://plugins.qgis.org/plugins/FlowMapper/version/0.4.1/
  • 62
    Bongiovanni S, Matos WH. Microbaciado córrego Jacu (Municípios de Assis e Cândido Mota, Oeste de São Paulo): Abordagem histórica, econômica e ambiental. [Internet]. Santa Catarina: Congresso Brasileiro de ciência e Tecnologia em Resíduos e desenvolvimento Sustentável; 2004;278-287 [updated 2018]. Available from: Available from: https://www.ipen.br/biblioteca/cd/ictr/2004/ARQUIVOS%20PDF/08/08-033.pdf/
    » https://www.ipen.br/biblioteca/cd/ictr/2004/ARQUIVOS%20PDF/08/08-033.pdf/
  • 63
    Saiani CCS, Toneto Júnior R. Evolution of the access to services of basic sanitation in Brazil (1970 to 2004). Econom Soc. 2010;19(1):79-106.
  • 64
    Fundação Sistema Estadual de Análise de Dados (SEADE). Informações dos municípios Paulistas. Portal de estatística do estado de São Paulo [Internet]. São Paulo: Fundação SEADE; 2016 [updated 2018]. Available from: Available from: http://www.imp.seade.gov.br
    » http://www.imp.seade.gov.br
  • 65
    Teles HMS. Ecological aspects of Biomphalaria Preston, 1910 in the State of Sao Paulo, Brazil. I. Syntopia. Cienc Cult. 1988;40(4):374-9.
  • 66
    Superintendência de Controle de Endemias (SUCEN). Boletim do Sistema de Vigilância Epidemiológico do ano de 1979-1980, do serviço Regional 11 - Marilia. Programa de Controle da Esquistossomose Mansônica no Estado de São Paulo, Secretaria de Estado da Saúde, SUCEN. 1980.
  • 67
    Superintendência de Controle de Endemias (SUCEN). Boletim do Sistema de Vigilância Epidemiológico do ano de 2009-2012, do serviço Regional 11 - Marilia. Programa de Controle da Esquistossomose Mansônica no Estado de São Paulo, Secretaria de Estado da Saúde, SUCEN. 2012.
  • 68
    Paraense WL. The schistosome vectors in the Americas. Mem Inst Oswaldo Cruz . 2001;96:7-16.
  • 69
    Figueiredo WSA, Epidemiologia da esquistossomose mansônica e o processo de organização espacial: o caso do município de Ourinhos, São Paulo. [São Paulo]: Faculdade de Saúde Pública-USP. Departamento de Epidemiologia. 2000: 40-52, 127-137 p.
  • 70
    Piroli VHB, Piroli EL. Deposição irregular de resíduos no leito das ruas de ourinhos e aumento das enxurradas e inundações. Periódico Eletrônico Fórum Ambiental da Alta Paulista. 2015;11(6):16-27.
  • 71
    Laurenti AEM, Piroli EL. Evolução do uso e ocupação do solo sobre as áreas de preservação permanente da microbacia urbana do córrego Christone 1972-2006 Ourinhos-SP. Rev Tópos. 2011;5(1):87-102.
  • 72
    Piroli EL, Ishikawa DTK, Demarchi JC. Análise das mudanças no uso do solo da microbacia do córrego das Furnas, município de Ourinhos-SP, entre os anos de 1972 e 2007, e dos impactos sobre suas áreas de preservação permanente, apoiada em geoprocessamento. Curitiba, Brasil: Simpósio Brasileiro de Sensoriamento Remoto, INPE; 2011;(15):6333-6340.
  • 73
    Guimarães MCDA, Menezes RMTD, Tuan R. Experimental study on reproduction of the freshwater snail Biomphalaria tenagophila (d’Orbigny, 1835). Invertebr Reprod Dev. 2016;60(2):145-51.
  • 74
    Paraense WL, Côrrea LR. Differential susceptibility of Biomphalaria tenagophila populations to infection with a strain of Schistosoma mansoni J Parasitol. 1978;64:822-6.
  • 75
    Guaraldo AMA, Magalhães LA, Rangel HDA, Pareja G. The evolution of sporocysts of Schistosoma mansoni, Sambon, 1907, in Biomphalaria glabrata (Say, 1818) and in Biomphalaria tenagophila (D'Orbigny, 1835). Rev Saude Publica . 1981;15(4):436-48.
  • 76
    Secretaria Nacional de Saneamento Ambiental (SNSA). Sistema Nacional de Informações sobre Saneamento. SNIS - Série Histórica [Internet]. Brasilia: Ministério das Cidades, SNSA;. 2015 [updated 2017; cited 2018]. Available from: Available from: http://app.cidades.gov.br/serieHistorica/
    » http://app.cidades.gov.br/serieHistorica/
  • 77
    Ludwig KM, Frei F, Alvares Filho F, Ribeiro-Paes JT. Correlation between sanitation conditions and enteroparasitoses in the population of Assis, Sao Paulo State, Brazil. Rev Soc Bras Med Trop . 1999;32(5):547-55.
  • 78
    Frei F, Juncansen C, Ribeiro-Paes JT. Epidemiological survey of intestinal parasite infections: analytical bias due to prophylactic treatment. Cad Saude Publica . 2008;24(12):2919-25.
  • 79
    Teixeira JC, Oliveira GSD, Viali ADM, Muniz SS. Study of the impact of deficiencies of sanitation on public health in Brazil from 2001 to 2009. Eng Sanit Ambient. 2014;19(1):87-96.
  • 80
    Perez MD, Santos MR, Ishihata JK. Contribution to the survey of the Planorbis map in the State of São Paulo; investigation of centres of Schistosoma mansoni infection in its evolutionary form.III. Hydrographic area of Assis-Cândido Mota (Paranapanema Valley). Hospital, Rio de Janeiro. 1968;74:495-507.
  • 81
    Menarin CA. Leituras do espaço e da política: elementos para uma história ambiental urbana. II colóquio da pós-graduação em letras “Literatura e Vida Social” UNESP, 2010: 267-282.
  • 82
    Brússolo RG, Ely DF. O clima e a cidade: Ilhas de calor em Assis/SP. Formação, 2015;2(22):99-127.
  • 83
    Rodrigues ACJ, Palmieri DA, Rodrigues RJ. Uso do geoprocessamento para planejamento, manejo e proteção de mananciais em áreas urbanas. Tekhne e Logos. 2018;9(1): 53-67.
  • 84
    Borda AA, Branco JR AC. Perfil físico-químico, microbiológico e ecológico de mananciais dágua na área urbana do município de Ipaussu, São Paulo. Salvador/BA IV: Congresso Brasileiro de Gestão Ambiental. 2013:1-9.
  • 85
    Silva LJ. Crescimento urbano e doença: a esquistossomose no município de São Paulo (Brasil). Rev Saude Publica . 1985;19(1):1-7.
  • 86
    Coura-Filho P. Schistosomiasis mansoni in urban territory. 2. A theoretical approach to the accumulation, concentration, and centralization of capital and the production of disease. Cad Saude Publica . 1997;13(3):415-24.
  • 87
    Coutinho JO, Pessôa SB. Sobre um foco autóctone da Esquistossomose mansonica em Jacarezinho (Norte do Paraná). Hospital, Rio de Janeiro. 1948;31(4):531-42.
  • 88
    Luz E, Silva SM, Carvalho AP, Castro N. Atualização da sistemática e de planorbídeos (Gasteropoda, Pulmonata) no Estado do Paraná (Brasil). Acta Biológica Paranaense. 1998;27.
  • 89
    Costa AB, Bravo DS, Guilherme TS, Marqui R, Silva FTR, Melo SCCS. Esquistossomose Urbana no Norte Pioneiro do Estado do Paraná, Brasil. J Health Sci, 2017;19(4):251-5.
  • 90
    Souza CPD, Caldeira RL, Drummond SC, Melo AL, Guimarães CT, Soares DDM, et al. Geographical distribution of Biomphalaria snails in the state of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz . 2001;96(3):293-302.
  • 91
    Eduardo MBP, Souza D, Ciaravolo RMC, Kanamura HY, Gargioni C, Falcão ACMG. Esquistossomose mansônica no Estado de São Paulo. Aspectos epidemiológicos. Bol Epidem Paul. 2005;18:2-8.
  • 92
    Bezerra IA. Situação da notificação em esquistossomose na Grande São Paulo (Brasil), no período de 1982 a 1983. Rev Saude Publica . 1984;18(5):386-95.
  • 93
    Ministério da Saude (MS), Portaria no1.399, de 15 de dezembro de 1999. Regulamenta a NOB SUS 01/96 no que se refere às competências da União, Estados, Municípios e Distrito Federal, na área de epidemiologia e controle de doenças, define a sistemática de financiamento. Brasília: MS , Diário Oficial da União; 1999, Seção 1.
  • 94
    Barbosa CS, Silva CBD, Barbosa FS. Esquistossomose: reprodução e expansão da endemia no Estado de Pernambuco no Brasil. Rev Saude Publica . 1996;609-16.
  • 95
    Wanderley DMV, Glasser CM, Silva B, Teles FB, 2006. Superintendência de Controle de Endemias-Sucen: 30 anos de trajetória. Suplemento especial, Bol Epidem Paul . 2006;3-9.
  • 96
    Centro de vigilância epidemiológica “prof. Alexandre Vranjac”. Vigilância epidemiológica e controle da esquistossomose: normas e instruções. São Paulo: CVE . 2007, 45 p.
  • 97
    Tibiriçá SHC, Guimarães FB, Teixeira MTB. A esquistossomose mansoni no contexto da política de saúde brasileira. Cien Saude Colet . 2011;16:1375-81.
  • 98
    Araujo ISD, Moreira ADL, Aguiar R. Doenças negligenciadas, comunicação negligenciada. Apontamentos para uma pauta política e de pesquisa. Rev Eletron Comun Inf Inov Saude. Rio de Janeiro. 2013;6(4).
  • Financial Support: The authors would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for providing doctoral fellowship for Raquel G.S. Palasio, the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for providing an undergraduate research project grant for Aline N. Bortoleto, and the Superintendence for the Control of Endemic Diseases (SUCEN) Head Office (Project nº 1819/2016) with grant to Roseli Tuan. CNPq for providing research productivity fellowship for Francisco Chiaravalloti-Neto (PQ-2, 307739/2016-3).

Publication Dates

  • Publication in this collection
    27 June 2019
  • Date of issue
    2019

History

  • Received
    06 Nov 2018
  • Accepted
    08 May 2019
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