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Revista da Sociedade Brasileira de Medicina Tropical

versão impressa ISSN 0037-8682versão On-line ISSN 1678-9849

Rev. Soc. Bras. Med. Trop. vol.52  Uberaba  2019  Epub 27-Jun-2019

http://dx.doi.org/10.1590/0037-8682-0447-2018 

Major Article

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

Raquel Gardini Sanches Palasio1  2 
http://orcid.org/0000-0003-1564-0871

Aline Nazaré Bortoleto2 

Iara Giordano Rosa-Xavier3 

Maria Teresa Macoris Andrighetti3 

Roseli Tuan2 

Francisco Chiaravalloti-Neto1 

1Programa de Pós-Graduação em Epidemiologia, Faculdade de Saúde Pública, Universidade de São Paulo, São Paulo, SP, Brasil.

2Laboratório de Bioquímica e Biologia Molecular, Superintendência de Controle de Endemias, São Paulo, SP, Brasil.

3SR11, Superintendência de Controle de Endemias, Marília, SP, Brasil.


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 disease1,2. It was reported that, in 2016, 12,411 adults were treated, and approximately 1.6 million individuals were infected with S. mansoni (Sm) in Brazil3,4. In 2012, positivity for Sm in Brazil was 4.5%5. 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)6.

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 measures5. 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 identified7-13.

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 Bahia14-15, Pernambuco16, Minas Gerais17-18, Recife19, and Sergipe20. Studies in areas with low endemicity of schistosomiasis, such as the state of SP, are rare. The studies by Anaruma Filho et al.21 and Teles et al.22 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 1952.23 Among the factors that could explain this autochthony would be the predominance and abundance of Biomphalaria glabrata.24-27 This species was found naturally infected with Sm for the first time in 1952 in Ourinhos.28-29 It has since been considered an important public health problem in this area of the state30-31. 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 IH32-35.

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)36-37 (Table 1), including GeoSentinel sites that are priorities for the surveillance of schistosomiasis38, which have a total estimated population of 488,955 inhabitants in 201839. These municipalities include a significant part of the autochthonous occurrence of schistosomiasis in the Middle Paranapanema region40. 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 River41-42.

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). 

Study periods
Municipalities Epidemiological 1º: 2º: 3º: 4º:
classification 1978-1988 1989-1999 2000-2006 2007-2016
N (%) N (%) N (%) N (%)
Ourinhos Autochthonous 963 (61.7) 414 (67.1) s.i. 25 (39.7)
Imported 472 (30.2) 115 (18.6) s.i. 5 (7.9)
Unknown origin 126 (8.1) 88 (14.3) 61 (100) 33 (52.4)
Assis Autochthonous 62 (13.1) 18 (29.5) s.i. 0 (0)
Imported 407 (86.2) 38 (62.3) s.i. 2 (100)
Unknown origin 3 (0.6) 5 (8.2) 1 (100) 0 (0)
Ipaussu Autochthonous 3 (10.7) 10 (37.0) s.i. 0 (0)
Imported 25 (89.3) 16 (59.3) s.i. 0 (0)
Unknown origin 0 (0) 1 (3.7) 3 (100) 0 (0)
Candido Mota Autochthonous 8 (4.6) 0 (0) s.i. 0 (0)
Imported 165 (94.3) 7 (87.5) s.i. 3 (100)
Unknown origin 2 (1.1) 1 (12.5) 7 (100) 0 (0)
Palmital Autochthonous 1 (1.6) 1 (5.6) s.i. 2 (66.7)
Imported 54 (88.5) 14 (77.8) s.i. 1 (33.3)
Unknown origin 6 (9.8) 3 (16.7) 0 (0) 0 (0)
Chavantes Autochthonous 0 (0) 1 (33.3) s.i. 1 (100)
Imported 54 (100) 2 (66.7) s.i. 0 (0)
Unknown origin 0 (0) 0 (0) 1 (100) 0 (0)
Canitar Autochthonous 0 (0) 0 (0) s.i. 1 (100)
Imported 9 (100) 4 (80.0) s.i. 0 (0)
Unknown origin 0 (0) 1 (20.0) 0 (0) 0 (0)
São Pedro Turvo Autochthonous 1 (2.4) 0 (0) s.i. 0 (0)
Imported 40 (97.6) 3 (100) s.i. 0 (0)
Unknown origin 0 (0) 0 (0) 2 (100) 0 (0)
*Others Autochthonous 0 (0) 0 (0) s.i. 0 (0)
Imported 656 (99.2) 95 (88.8) s.i. 2 (33.3)
Unknown origin 5 (0.8) 12 (11.2) 20 (100) 4 (66.7)
Total Autochthonous 1038 (33.9) 444 (52.3) s.i. 29 (36.7)
Imported 1882 (61.5) 294 (34.6) s.i. 13 (16.5)
Unknown origin 142 (4.6) 111 (13.1) 95 (100) 37 (46.8)

Source: SUCEN and SINAN. *Other municipalities of GeoSentinel sites of Middle Paranapanema with cases = Bernardino de Campos, Borá, Cruzália, Espírito Santo do Turvo, Florínia, Ibirarema, Lutécia, Maracaí, Óleo, Paraguaçu Paulista, Pedrinhas Paulista, Platina, Ribeirão do Sul, Salto Grande, Santa Cruz do Rio Pardo, Tarumã, and Timburi. s.i., no information.

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)43-47 and the Secretariat for the Environment of the State of SP48.

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 tool49, and the points corresponding to the geographical coordinates were imported in the format of latitude/longitude (datum WGS84) into the software QGIS version 2.1450.

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 MMQGIS51 in QGIS50. The areas at greatest risk for schistosomiasis were identified using the spatial scan statistics in SaTScan version 9.452. 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 clusters53-54. 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 Health55. The snails were identified by examination of the morphological characteristics of their reproductive apparatus as described in Paraense56-57. All snails were exposed to artificial light in the laboratory to induce shedding of trematode cercariae of Sm55.

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-function58, in the R software version 3.2.259 with Splancs package60. 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 package60 in the R software59.

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 0.4.161 tool, an extension of QGIS50.

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.  

Municipalities Water Bodies *Bgl *Btt Boc Bpe N° snails collected Latitude Longitude Collection date
Ourinhos Christoni x 212 -22.967600 -49.874683 2015-2016
x 46 -22.967117 -49.875167 2015-2017
x 146 -22.964467 -49.875633 2015-2016
x x 147 -22.952833 -49.876333 2015-2016
x x 77 -22.950050 -49.875850 2015-2016
Furninhas x x 175 -22.985556 -49.849972 2015-2016
x 109 -22.977056 -49.851667 2015-2017
x 32 -22.976766 -49.851745 2015
Assis Fortuninha x 20 -22.660240 -50.437510 2017
Jacu x x 24 -22.670850 -50.406117 2017
Ipaussu São Luiz (Sapo) x x 149 -23.064750 -49.630250 2015-2016
x x 114 -23.060083 -49.628333 2015-2016
x 23 -23.047528 -49.630250 2015-2016
x x 113 -23.046556 -49.627528 2015-2016
x 86 -23.045750 -49.625250 2015-2016

*All specimens of IH were negative for the elimination of S. mansoni cercariae. Bgl, B. glabrata (Say, 1818); Btt, B. tenagophila (d’Orbigny, 1835); Boc, B. occidentalis (Paraense, 1981); Bpe, B. peregrina (d’Orbigny, 1835).

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 Assis62), 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 municipalities6,63,64 and/or the appropriate treatment of patients34. 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 transmission19.

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. glabrata27,65-67, 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 parasite29,68. 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 flooding70, with vegetable gardens in meadows71 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. glabrata27,66 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)72, 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 environments73 and has a limited capacity to act as an IH of Sm74,75.

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 treated76. 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 present55. 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 infection69. Our results corroborate the findings of other authors65,85,86 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 treated76. 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 Assis77,78, demonstrating the impact of basic sanitation on intestinal infectious diseases6,79. Although the Fortuninha stream is still colonized by B. glabrata66,80, it has been channeled, and lakes have been constructed, making it a public park81. The same has happened to the Jacu stream, that has undergone changes in width and depth, recomposition of the gallery forest82, and channeling in its urban stretch83, conditions that must have favored the replacement of B. glabrata66,80by 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. glabrata66, sometimes found infected with Sm31,66. Currently, the levels of fecal coliforms in the São Luiz stream are within the levels allowed by law84, 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 200327,67, 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 Figueiredo69 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 194887 and has the presence of B. glabrata88 and B. tenagophila55,89. 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. glabrata5,30,85,90. Possibly, this disease was introduced in SP, just as in Paraná, by infected immigrants from Minas Gerais and the Northeastern region of the country85.

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.91, 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 Bezerra92, 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 19995,93. 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 activities5,94-96. Underreporting contributes to the characterization of schistosomiasis as a neglected tropical disease, which is not accorded priority by public health policies34,97,98.

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.

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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).

Recebido: 06 de Novembro de 2018; Aceito: 08 de Maio de 2019

Corresponding author: Raquel Gardini Sanches Palasio. e-mail: raquelpalasio@usp.br

Conflict of Interest: The authors declare that there is no conflict of interest.

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