Parasitology Research (2018) 117:1495–1502 https://doi.org/10.1007/s00436-018-5810-1

ORIGINAL PAPER

Spatial distribution and seasonality of spp. in São Luís (Maranhão, Brazil)

Nathalia Ferreira David1 & Selma Patrícia Diniz Cantanhede2 & Natanael Bezerra Monroe3 & Luciana Patrícia Lima Alves Pereira4 & Nêuton Silva-Souza5 & Ana Lúcia Abreu-Silva3,4 & Verônica Maria de Oliveira2 & Ligia Tchaicka2

Received: 26 June 2017 /Accepted: 14 February 2018 /Published online: 17 March 2018 # Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract Two of the three vector of mansoni Sambon, 1907 in Brazil occur in the state of Maranhão: (Say, 1818) and (Dunker, 1848). For the implementation of effective measures to combat schistosomiasis, it is necessary to identify the spatial and seasonal dynamics of these snails. Therefore, this work brought together information from malacological survey carried out in São Luís (Maranhão, Brazil) to identify the spatial and seasonal distribution patterns of Biomphalaria spp. snails. We used data from malacological surveys of the Municipal Health Secretary of São Luís, conducted between 2006 and 2013 in 23 neighborhoods. We also used data from the mollusk surveys that we conducted for 2 years (2012–2014) in four of these neighborhoods. During the 8-year period (2006–2013), 15,990 specimens of Biomphalaria spp. were collected. There was a positive association between precipitation and the abundance of mollusks of the genus Biomphalaria. During 2012–2014, a total of 2487 snail specimens were obtained (B. glabrata:1046specimens;B. straminea: 1426 specimens). There was a positive correlation between precipitation and B. straminea abundance. High density of human occupation and high precipitation are two factors that affect the distribution and density of Biomphalaria spp. populations.

Keywords Schistosomiasis . Freshwater snails . Biomphalaria glabrata . Biomphalaria straminea . Malacology

Introduction

Snails of the genus Biomphalaria inhabit environments with * Ligia Tchaicka lentic or lotic freshwater (Medeiros et al. 2002; Pordeus et al. [email protected] 2008) and survive in anthropized regions (Medeiros et al. 2002) such as residential areas. Some of the species have 1 Programa de Pós-Graduação em Biodiversidade e Conservação, Universidade Federal do Maranhão, Av. dos Portugueses, 1966, Vila epidemiological significance and the interaction of these Bacanga, São Luís, MA 65080-805, Brazil snails with the urban environment is related to a major public 2 Programa de Pós-Graduação em Recursos Aquáticos e Pesca, health problem, i.e., schistosomiasis (Barbosa et al. 2000; Departamento de Química e Biologia, Universidade Estadual do Cantanhede 2015). The presence and maintenance of suscep- Maranhão, Cidade Universitária Paulo VI, s/n, Tirirical, São tible strains of these vectors favor the continuity of schistoso- Luís, MA 65055-970, Brazil miasis in endemic regions, as well as its introduction to non- 3 Programa de Pós-Graduação em Ciência , Departamento de endemic areas (Telles 2005). Ciências Agrárias, Universidade Estadual do Maranhão, Cidade Thirty-four species of Biomphalaria have been described Universitária Paulo VI, s/n, Tirirical, São Luís, MA 65055-970, Brazil worldwide, inhabiting the tropics and subtropics. Twenty-two of these species occur in the Americas, and the other 12 spe- 4 Programa de Pós-Graduação em Biotecnologia da Rede Renorbio, Universidade Federal do Maranhão, Av. dos Portugueses, 1966, Vila cies are found in Africa and the Middle East (Chitsulo et al. Bacanga, São Luís, MA 65065-545, Brazil 2000; Dejon et al. 2001;Gryseelsetal.2006; Steinmann et al. 5 Departamento de Química e Biologia, Universidade Estadual do 2006). Ten species and one subspecies have been identified in Maranhão, Cidade Universitária Paulo VI, s/n, Tirirical, São Brazil (Paraense 1975, 1981, 1984, 1988; Carvalho et al., Luís, MA 65055-970, Brazil 2008a; Thiengo and Fernandez 2008). 1496 Parasitol Res (2018) 117:1495–1502

Among the three Biomphalaria species found naturally in- Municipal Health Department of São Luis (Maranhão, fected by Sambon, 1907, Biomphalaria Brazil). These data are the information on the location of the glabrata (Say, 1818) is the most important intermediate host snails (neighborhood), date, presence/absence of the snail in in the Americas, owing to its great compatibility with the the breeding sites, and the number of snails collected and were parasite (Souza et al. 1998) and its (1999), which describes manually recorded in tables by health agents during the cap- the distribution of biological diversity in the Brazilian territory ture of snails. (Carvalho et al. 2008b), the development of different types of According the health department, sites with natural water climates, and a variety of permanent breeding sites (Paraense bodies in each neighborhood were inspected and designated 2008). (D'Orbigny, 1835) has a as collection points and were treated as breeding sites when more restricted distribution to the southern and south- the presence of mollusks was verified. Based on this catego- eastern states, and has epidemiological importance in rization, the frequency of the breeding sites (frequency of the transmission of S. mansoni in the states of these water bodies with snails) was calculated by the ratio the num- regions (Carvalho et al., 2008b). ber of freshwater collections with Biomphalaria and the total Schistosomiasis is endemic to tropical areas, has a wide geo- number of freshwater collections surveyed, multiplied by 100. graphical distribution, and is reported in more than 76 countries Snails were captured annually using the Baleatory scoops^ (Santos and Melo 2011). In Brazil, it is one of the most relevant technique (Olivier and Schneiderman 1956) (ten aleatory parasitic endemic diseases (Enk et al. 2010); its occurrence is scoops per collection point) and identified genus level by ex- maintained owing to deficiencies in basic sanitation and environ- ternal morphology (shell characteristics). The studied neigh- mental education among the population. It is among the most borhoods are indicated in Fig. 1. prevalent waterborne diseases (Gubler 1989; Vitorino et al. 2012). Considering the characteristics of population occupation, The transmission and manifestation of schistosomiasis are the 23 neighborhoods investigated were grouped in geograph- more frequent in the northeastern regions of Brazil (Resendes ic areas: northern region ( = average and recent human oc- et al. 2005; Araújo et al. 2007), but its occurrence is consid- cupation northern region), mid-northeastern region ( =in- erably widespread in the southeastern states as well (Lara et al. tense occupation, old and disorderly), northwestern region 2013). In Maranhão, schistosomiasis has been recorded since ( = intense occupation, old and disorderly), mid-southern 1920 (Coura and Amaral 2004), with high prevalence in the region ( = little occupation), and southern region ( = little north coast and northwestern region (Resendes et al. 2005). occupation). Biomphalaria species found in Maranhão include B. glabrata, The collection points of snails were plotted on satellite B. straminea,andBiomphalaria schrammi (Crosse, 1864) images obtained from Google Earth to create a map using (Carvalho et al. 2008a;Cantanhede2015). the program, ArcGIS 10.3. In São Luís (capital of Maranhão), a city located in the coastal The relationship between the mean annual precipitation region of the state, there are occurrences of S. mansoni vectors in (mm) and the total number of Biomphalaria snails obtained peripheral neighborhoods, and the precarious sanitary conditions in each year was tested. For this purpose, the Pearson correla- of these neighborhoods make the city an interesting subject of tion coefficient was used, and p values < 0.05 were considered study for the epidemiology of schistosomiasis. statistically significant. The values of precipitation are coming Knowing the potential factors behind the establishment of from the meteorological station of São Luís—A203 schistosomiasis as a major public health problem is extremely (2.526771° S, 44.213577° W) and were provided by the important in order to create strategies for epidemiological sur- Center for Meteorological Research at Universidade veillance. Precise identification of Biomphalaria spp. in the Estadual do Maranhão. areas of possible transmission and knowledge of the distribu- Another survey carried out over 2 years (2012–2014), for tion patterns of planorbids are crucial aspects for planning the neighborhoods of São Luis, was investigated: Barreto (E), control of vector snail populations. Therefore, this study Coroadinho (J), Sá Viana (L), and Vila Jambeiro (N) (Fig. sought to compile information from malacological sur- 1). The breeding sites of snails were selected for each neigh- veys carried out in São Luís (Maranhão, Brazil) to iden- borhood. The selection criterion was based on the report of tify the spatial and seasonal distribution patterns of vec- actions of the control program of schistosomiasis of the tor snails and assist in the planning of control strategies Municipal Health Department of São Luis which classified for schistosomiasis. several neighborhoods as areas of risk in São Luís, due to the concentration of the cases of schistosomiasis during 2006–2013. Materials and methods Snail collection was carried out every 2 months, in a delimited area of 4 m2. A standardized methodology of We used the breeding site data for Biomphalaria from an 8- ten shells followed by 10 min of active search for snails year period (2006–2013), which were provided by the was used. All the captured snails were identified using Parasitol Res (2018) 117:1495–1502 1497

Fig. 1 Map of São Luís, Maranhão (Brazil), emphasizing the regions Nice Lobão, L. Sá Viana, M.Gapara,N. Vila Jambeiro, O. Vila Embratel, (geometric symbols) and the 23 districts investigated (letters) for the P. Vila Conceição, Q. Vila Esperança, R. São Cristovão, S.Maracanã,T. presence of Biomphalaria spp. breeding sites, from 2006 to 2013. The Vila Nova República, U. Pedrinhas, V. Bacabal, and W. Itapera. The dotted lines delimit the area of study in northern and southern regions. neighborhoods are grouped into geographic regions: northern region The arrows indicate the four collection sites (breeding sites) sampled in ( = average and recent human occupation), mid-northeastern region the 2-year survey (2012–2014). A. Vila Luizão, B. Rio Grande, C. ( = intense occupation, old and disorderly), northwestern region Coquilho, D. Residencial Primavera, E.Barreto,F. Areinha, G.Monte ( = intense occupation, old and disorderly), mid-southern region H I J K Castelo, . Salina do Sacavém, . Coroado, .Coroadinho, .Parque ( = little occupation), and southern region ( = little occupation)

shell characteristics, and a sample of 10% specimens Results from each breeding place was identified using internal anatomical characteristics: presence/absence of the renal During the 8-year period (2006–2013), the Municipal Health crest and vaginal wrinkling (Deslandes 1951;Rey1955; Department investigated 250 neighborhoods, and 153 of them Paraense 1975, 1981).Thesamesnailswerealsosub- were found to be breeding sites of Biomphalaria. In total, mitted for molecular identification using restriction frag- there were 550 breeding sites and 15,990 snails collected. In ment length polymorphism–polymerase chain reaction the 23 neighborhoods (Fig. 1) that were visited every year, (PCR–RFLP) for the intragenic spacer ITS, as described 212 breeding sites were registered. by Vidigal et al. (1998). Considering the frequency of breeding sites categorized by The Pearson correlation coefficient was calculated with a geographic area, the mid-northeastern and northwestern areas significance level of p < 0.05 in order to investigate the rela- showed a higher occurrence of Biomphalaria breeding sites tionship between the average monthly rainfall (mm) and the (51.0 and 44.2%, respectively), whereas in the mid-southern, number of snails of each species (B. glabrata and southern, and northern regions, breeding sites were less fre- B. straminea) captured each month. All statistical analyses quent (1.3, 0.0, and 3.3%, respectively). were performed using the R statistical software (R Core Figure 2 shows the relationship between annual mean pre- Team 2016). cipitation and number of Biomphalaria snails. A strong 1498 Parasitol Res (2018) 117:1495–1502

Fig. 2 Number of Biomphalaria snails and the average annual precipitation (mm) between 2006 and 2013, São Luís, Maranhão, Brazil

significant positive association was found between the num- In Sá Viana, B. glabrata and B. straminea were verified as ber of Biomphalaria snails and the annual mean precipitation inhabiting the same breeding sites (stream with sewage). (r =0.9224;p = 0.0413) (Fig. 3). From the correlation analysis between average monthly During the survey of the four neighborhoods (2012–2014), precipitation and the number of snails by species 2487 snails were collected. According to the morphological (B. glabrata and B. straminea), we obtained the following identification (shells and anatomy), we obtained 1046 speci- results: (A) Sá Viana B. straminea (r = − 0.4520; p =0.001), mens of B. glabrata and 1426 specimens of B. straminea. B. glabrata (r = − 0.2456; p =0.2856),(B)VilaJambeiro Molecular analyses confirmed the specific identification. B. straminea (r = 0.7119; p = 0.004), (C) Coroadinho B. straminea was verified in the four monitored breeding sites. B. straminea (r = 0.7556; p = 0.0010), and (D) Barreto B. straminea (r =0.8018;p = 0.0008). Figure 4 shows the av- erage monthly precipitation and the number of specimens of B. glabrata and B. straminea collected in each of the four neighborhoods between 2012 and 2014. The mean monthly precipitation shows a strong and signif- icant positive association with the number of B. straminea obtained in B, C, and D. For the specimens of B. straminea obtained in A, the statistical analysis was significant, but it showed a negative correlation and low explanatory value with respect to precipitation. There was no statistically significant association for B. glabrata.

Discussion

Our results indicate that areas near Bacanga River Basin (mid- northeastern and northwestern region) presented a high fre- quency of breeding sites for Biomphalaria. The establishment Fig. 3 The Pearson correlation for Biomphalaria snails and the average and territorial expansion of Biomphalaria spp. populations is annual precipitation (mm) between 2006 and 2013, São Luís, Maranhão, Brazil historically related to river basin regions (Carvalho et al. 1985; Parasitol Res (2018) 117:1495–1502 1499

Fig. 4 Number of B. glabrata and B. straminea (collected in: A. Sá Viana, B. Vila Jambeiro, C. Coroadinho, and D. Barreto) and the mean monthly precipitation (mm) between 2012 and 2014, São Luís, Maranhão, Brazil

Telles 1996; Fernandez et al. 2001; Telles 2005;Lofty2009; However, the results suggest that presence of a hydrographic El-Wakeil et al. 2013;Abou-el-Naga2015; Leite et al. 2016). basin is not the primary determinant of breeding site frequency, 1500 Parasitol Res (2018) 117:1495–1502 since the southern and mid-southern regions present low fre- In addition to influencing the distribution and density of quency of breeding sites despite having considerable hydro- snails, the rainy season might also facilitate the transmission graphic basins. The occupation by snails is more strongly related of schistosomiasis. In a malacological survey carried out in to the characteristics of human occupation in the area. There is a Pernambuco (Brazil), all snails positive for S. mansoni were high concentration of snail breeding sites in urbanized territories, found during the rainy season (Oliveira et al. 2013). Similar where the neighborhoods have a high population density, with results were found in Senegal (Africa) for Biomphalaria intense occupation, and are old and disorderly. In these areas, the pfeifferi (Krauss, 1848) (Ernould and Sellin 1999). construction of irregular houses advanced on the mangrove veg- During our 2-year survey (2012–2014), we collected more etation, resulting in environmental degradation (Nascimento specimens of B. straminea than of B. glabrata. In addition, 2010; Ribeiro et al. 2014). The process of urbanization and its B. straminea was verified in all four of the monitored breeding characteristics as the form of territorial occupation and environ- sites. Although B. glabrata is considered the most efficient mental degradation are also indicated as factors determining the intermediate host for S. mansoni (Paraense 1972;Guimarães occurrence of snail breeding sites and, consequently, as a risk for and Tavares-Neto 2006), B. straminea presents great abundance the transmission of schistosomiasis (Patz et al. 2000;Gomes and wide geographical distribution, occurring in permanent and et al. 2012;Moraesetal.2014;Abou-el-Nagaetal.2015; temporary breeding sites from the north to the south of Brazil Barbosa et al. 2015; Loyo and Barbosa 2016). (Paraense 2008), owing to its greater ability of adaptation to all Although this parasitic disease is predominantly reported in varieties of climate and ecological conditions (Paraense 1972). individuals living in rural areas (Githeko et al. 2000;Dejongetal. The record of B. glabrata and B. straminea inhabiting the 2001; Abou-el-Naga et al. 2015), since 1990, cases of schistoso- same sewage stream shows the need for efficient analyses for miasis have been recorded in urban and coastal areas of Brazil as taxonomic identification. Juvenile specimens are often obtained well (Gonçalves et al. 1991;Barbosa2001;Araujoetal.2007). from breeding sites, but their differentiation is difficult. The The spread of schistosomiasis as an urban endemic disease simultaneous occurrence of these two species of Biomphalaria has also been observed in South America, North Africa (Egypt), has been recorded in nearby breeding sites, indicating a syntopic and Asia (Honk Kong and Vietnam), where more than 70% of relationship (Telles 1996; Oliveira et al. 2013; Loyo and the population already resides in urban areas. These regions are Barbosa, 2016). However, in our study, the two species were undergoing disordered growth of the cities, owing to the popu- found inhabiting the same breeding sites in neighborhood A, lation seeking work in urban regions (Githeko et al. 2000). suggesting sympatry. This was has also been reported in São Regarding the association between precipitation and popula- Luís in the neighborhood of Vila Embratel (Oliveira et al. 2013). tion density of Biomphalaria spp., some studies have reported a In the Republic of Kenya (Africa), simultaneous occur- negative correlation between these variables for torrential rains. rences of Biomphalaria choanomphala (Martens, 1879) and The increase of rainfall causes water to flow out of the breeding (Martens, 1870) on the coast of Lake sites, causing a drag effect and reduction in snail numbers. Thus, Victoria and of and B. sudanica in the the snails are dispersed and the new foci of these vectors are Chebwonyo Dam reservoir have been registered (Bandoni formed in other localities (Giovanelli et al. 2001;Araujoetal. et al. 2000). Plam et al. (2008) also reported simultaneous 2007; Souza et al. 2010; Barbosa et al. 2015). occurrence for four species in Lake Albert (Uganda): In our study, a positive association was observed between B. choanomphala, B. pfeifferi, B. sudanica,and the mean values of precipitation and number of mollusks of Biomphalaria stanleyi (Smith, 1888). Biomphalaria genus, specifically for B. straminea.Itispossi- Only in neighborhood A, the relation between precipitation ble that weak rains would have contributed to the proliferation and expansion of B. straminea was not significant. This fact of breeding sites, but did not cause dispersal of snails to other may be related to interspecific competition and emphasizes localities, since there were irregularities in the rainfall pattern the importance of detailed studies investigating the ecological in São Luís (Maranhão) in recent years (Miranda et al. 2016). factors underlying simultaneous occurrences of B. glabrata Some studies found that during rains, there is a demographic and B. straminea in natural environment, as well as other explosion of snails in estivation in temporary breeding sites, vector species. along with a higher peak of reproduction of these In summary, our results suggest that high density of human (Rumi and Hamann 1992; Barbosa and Barbosa 1994; Brooker occupation and high precipitation are both factors that influence et al. 2002; Souza et al. 2008; Oliveira and Assis 2012). the expansion and density of the populations of Biomphalaria, Our result showing a directly proportional relationship be- especially of B. straminea. We believe that the results presented tween increased precipitation and increased occurrence of here reflect the specific situation of not only Biomphalaria spp. Biomphalaria spp. has already been verified for breeding sites in São Luís (Maranhão) but also of other urban B. straminea (Buchmman 2014)andB. glabrata (Souza areas that underwent disordered space occupation and environ- et al. 2010;Oliveiraetal.2013; Cantanhede 2015; Miranda mental degradation. These factors should be considered when et al. 2016). planning control strategies for schistosomiasis. Parasitol Res (2018) 117:1495–1502 1501

This information is relevant for understanding the transmis- Carvalho OS, Amaral RS, Dutra LV,Scholte RGC, Guerra MAM (2008a) sion dynamics of schistosomiasis in other endemic and non- Distribuição espacial de Biomphalaria glabrata, B. straminea e B. tenagophila, hospedeiros intermediários do Schistosoma mansoni endemic localities and for the monitoring of snail breeding no Brasil. In: Carvalho OS, Coelho PMZ, Lenzi H (eds) sites. Monitoring the breeding sites, along with other interven- Schistosoma mansoni and Esquistossomose: uma visão tions (improvements in sanitation, water supply, and health multidisciplinar. Editora Fiocruz, Rio de Janeiro, pp 393–418 education), should continue to be implemented as a strategy Carvalho OS, Guimarães CT, Massara CL, Bonesio JER (1985) Situação atual da esquistossomose mansoni no lago da Pampulha, Belo to reduce the transmission of schistosomiasis. Horizonte, MG, Brasil. Rev Saude Publica 19:270–277 Carvalho OS, Jannotti-Passos LK, Caldeira RL (2008b) Importância Acknowledgments We would like to acknowledge the Conselho epidemiológica e biologia molecular aplicada ao estudo dos Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and moluscos do gênero Biomphalaria. In: Carvalho OS, Coelho Fundação de Amparo a Pesquisa e ao Desenvolvimento Científico do PMZ, Lenzi HL (eds) Schistosoma mansoni and Esquistossomose: Maranhão (FAPEMA) for granting the scientific initiation grant. Thanks uma visão multidisciplinar. Fiocruz, Rio de Janeiro, pp 311–345 are also due to the Secretaria Municipal de Saúde de São Luís (SEMUS) Chitsulo L, Engels D, Montresor A, Savioli L (2000) The global status of for providing us the data. This research did not receive any specific grant schistosomiasis and its control. Acta Trop 77:41–51 from funding agencies in the public, commercial, or not-for-profit sectors. Coura JR, Amaral RS (2004) Epidemiological and control aspects of schistosomiasis in Brazilian endemic areas. Mem Inst Oswaldo Compliance with ethical standards Cruz 99:13–19 Dejong RJ, Morgan JAT, Paraense WL, Pointier JP, Amarista M, Ayeh- Kumi PFK (2001) Evolutionary relationships and biogeography of Conflict of interest The authors declare that they have no conflict of Biomphalaria (: ) with implications regard- interest. ing its role as host of the human bloodfluke, Schistosoma mansoni. MolBiolEvol18:2225 –2239 Deslandes N (1951) Técnica de dissecção e exame de planorbídeos. Rev References Saude Publica 4:371–382 El-Wakeil KFA, Obuid-Allah AH, Mohamed AH, El FEZAA (2013) Community structure of molluscans in River Nile and its branches Abou-el-Naga I (2015) Demographic, socioeconomic and environmental in Assiut governorate, Egypt. Egypt J Aquat Res 39:93–198 changes affecting circulation of neglected tropical diseases in Egypt. Enk MJ, Amaral GL, Silva MF, Silveira-Lemos D, Teixeira-Carvalho A, Asian Pac J Trop Biomed 8:881–888 Martins-Filho A (2010) Rural tourism: a risk factor for schistosomi- Abou-el-Naga IF, Sadaka HA, Amer EI, Diab IH, Khedr SI (2015) Impact of asis transmission in Brazil. Mem Inst Oswaldo Cruz 105:537–540 the age of snails on Schistosoma mansoni Ernould JC, Sellin B (1999) The impact of the local water development transmission: modulation of the genetic outcome and the internal de- programme on the abundance of the intermediate hosts of schisto- fence system of the snail. Mem Inst Oswaldo Cruz 110:585–595 somiasis in three villages of the Senegal River delta. Liverpool Sch Araújo KCGM, Resendes APC, Souza-Santos R, Júnior JCS, Barbosa CS Trop Med 93:135–145 (2007) Análise espacial dos focos de Biomphalaria glabrata edecasos Fernandez MA, Thiengo SC, Boaventura MF (2001) Gastrópodes humanos de esquistossomose mansônica em Porto de Galinhas, límnicos do Campus de Manguinhos, Fundação Oswaldo Cruz, Pernambuco, Brasil, no ano 2000. Cad Saude Publica 23:409–417 Rio de Janeiro, RJ. Rev Soc Bras Med Trop 34:279–282 ’ Bandoni SM, Mulvey M, Loker ES (2000) Population structure and tax- Giovanelli A, Soares MS, D andréa SP, Gonçalves MML, Rey L (2001) onomic discrimination among three species of Biomphalaria Abundância e infecção do molusco Biomphalaria glabrata pelo Preston, 1910 (Gastropoda: Planorbidae) from Kenya. Zool J Schistosoma mansoni no estado do Rio de Janeiro. Rev Saude – Linnean Soc 129:387–401 Publica 35:523 530 Barbosa CS, Pierib OS, Silvac CB, Barbosa FS (2000) Ecoepidemiologia Githeko AK, Lindsay SW, Confalonieri UE, Patz JA (2000) Climate change and vector-borne diseases: a regional analysis. Bull World da esquistossomose urbana na ilha de Itamaracá, Estado de Pernambuco. Rev Saude Publica 34:337–341 Health Organ 78 Gomes ECS, Leal-Neto OB, Albuquerque J, Silva HP, Barbosa CS Barbosa CS, Santos RS, Gomes ES, Araújo K, Albuquerque J, Melo F, (2012) Schistosomiasis transmission and environmental change: a Guimarães RJ (2015) Epidemiologia da esquistossomose no litoral spatiotemporal analysis in Porto de Galinhas, Pernambuco-Brazil. de Pernambuco. Rev Patologia Tropical 43:436–445 Int J Health Geogr 11:51 Barbosa FS (2001) Tópicos em malacologia médica. Fiocruz, Rio de Gonçalves JF, Santana W, Barbosa CS, Coutinho A (1991) Janeiro Esquistossomose aguda, de caráter episódico, na Ilha de Itamaracá, Barbosa FS, Barbosa CS (1994) The bioecology of snail vectors for estado de Pernambuco. Cad Saude Publica 7:424–425 – schistosomiasis in Brazil. Cad Saude Publica 10:200 209 Gryseels B, Polman K, Clerinx J, Kestens L (2006) Human schistosomi- Brooker S, Beasley M, Ndinaromtan M, Madjiouroum EM, Baboguel M, asis. Lancet 368:1106–1118 Djenguinabe E, Hay SI, Bundy DA (2002) Use of remote sensing Gubler DJ (1989) Surveillance for dengue and dengue hemorrhagic fever. and a geographical information system in a national helminth con- Bull Org Panam 23:397–494 trol programme in Chad. Bull World Health Organ 80:783–789 Guimarães ICS, Tavares-Neto J (2006) Transmissão urbana de Buchmann FF (2014) Malacofauna límnica do reservatório da Usina esquistossomose em criança em um bairro de Salvador, BA. Rev Hidrelétrica de Cana Brava-GO, com ênfase em Biomphalaria Soc Bras Med Trop 39:451–455 straminea (Dunker, 1848), transmissora natural da Esquistossomose. Lara FV, Freitas J, Carvalho J, Carlos L, Alves M, Silva S, Vilaça VC, Dissertação de mestrado, Fundação Oswaldo Cruz Amaral RM (2013) Esquistossomose, uma doença no contexto da Cantanhede SPD (2015) Gastrópodes límnicos e helmintofauna associada saúde pública brasileira. Nova Rev Cient 2:1–15 da Microrregião da Baixada Maranhense, MA, com ênfase nos Leite MGP, Pimenta EC, Fujaco MAG, Eskinazi-Sant’Anna EM (2016) transmissores da esquistossomose. Tese de doutorado, Fundação Irrigation canals in Melo creek basin (Rio Espera and Capela Nova Oswaldo Cruz municipalities, Minas Gerais, Brazil): habitats to Biomphalaria 1502 Parasitol Res (2018) 117:1495–1502

(Gastropoda: Planorbidae) and potential spread of schistosomiasis. Uganda, show homoplasies in shell morphology. Zool Soc S Braz J Biol 76:638–644 Africa 43:34–44 Lotfy WM (2009) Human schistosomiasis in Egypt: historical review, Pordeus LC, Aguiar LR, Quinino LRM, Barbosa CS (2008) A ocorrência assessment of the current picture and prediction of the future trends. das formas aguda e crônica da esquistossomose mansônica no Brasil J Med Res Inst 30:1–7 no período de 1997 a 2006: uma revisão de literatura. Epidemiol Loyo RM, Barbosa CS (2016) Bioindicadores para avaliação do risco Serv Saude 17:163–175 potencial de transmissão da esquistossomose no açude Apipucos, Resendes APC, Souza-Santos R, Barbosa CS (2005) Internação e Pernambuco. Rev Ambient Água 11:146–161 mortalidade por esquistossomose mansônica no estado de Medeiros AS, Cruz OJ, Fernandez MA (2002) Esquistossomose Pernambuco, Brasil, 1992/2000. Cad Saude Publica 21:1392–1401 mansônica e distribuição dos moluscos límnicos em criadouros Rey L (1955) Técnicas de dissecção empregadas no estudo dos naturais no Município de Niterói, Rio de Janeiro, Brasil. Cad planorbídeos vetores da esquistossomose. Clinics 10:293–297 – Saude Publica 18:1463 1468 Ribeiro LMS, Silva MHS, Carvalho TSV (2014) A EVOLUÇÃO DO Miranda GS, Rodrigues JGM, Lira MGS, Nogueira RA, Gomes GCC, USO E OCUPAÇÃO DO ESPAÇO URBANO EM SÃO LUÍS: um Miranda BS, Araújo A, Silva-Souza N (2016) Moluscos límnicos estudo de caso da sub-bacia do Rio das Bicas. In: Anais Eletrônicos como hospedeiros de trematódeos digenéticos de uma região do Congresso Brasileiro de Geógrafos, Vitória, ES-Brasil – metropolitana da ilha do Maranhão, Brasil. Scientia Plena 12:1 11 Rumi A, Hamann MI (1992) Spatial and seasonal trends of a natural Moraes CN, Bichara CNC, Pontes NA, Pinto SCA, Gasparetto D (2014) population of Biomphalaria ocidentallis in northeastern Argentina. Correlação de criadouros de Biomphalaria sp., hospedeiro do Mem Inst Oswaldo Cruz 87:181–186 Schistosoma mansoni, em área de baixa infraestrutura sanitária no – Santos AM, Melo ACFL (2011) Prevalência da esquistossomose num Distrito de Mosqueiro, Belém, Pará. Hygeia. Media 10:216 233 povoado do município de Tutóia, estado do Maranhão. Rev Soc Nascimento JD (2010) O índice de sustentabilidade ambiental do uso da Bras Med Trop 44:97–99 água como ferramenta de contribuição às políticas públicas de Souza CP, Lima LC, Passos LKJ, Ferreira SS, Guimarães CT, Vieira LBF, desenvolvimento e conservação na bacia do rio Bacanga, São Junior RM (1998) Moluscos límnicos da microrregião de Belo Luis, MA. Dissertação de mestrado, Universidade Federal do Horizonte, MG, com ênfase nos vetores de parasitoses. Rev Soc Maranhão Bras Med Trop 31:449–456 Oliveira DS, Nunes GS, Mendes RJ, França CRC, Filho AAP, Tavares CP, Souza MAA, Barbosa VS, Albuquerque JO, Bocanegra S, Souza-Santo Rosa IG (2013) Inquérito malacológico para identificar a célula de SR, Paredes H, Barbosa CS (2010) Aspectos ecológicos e expansão da esquistossomose mansônica na Vila Embratel, um bairro levantamento malacológico para identificação de áreas de risco para da periferia de São Luís do Maranhão. Cad Pesquisa 20:25–32 transmissão da esquistossomose mansoni no litoral norte de Oliveira VN, Assis CRD (2012) Doenças tropicais negligenciadas na Pernambuco, Brasil. Iheringia Ser Zool 100:19–24 região nordeste do Brasil. Scire Salut 2:29–48 Olivier L, Schneiderman MA (1956) A method for estimating the density Souza MAA, Barbosa VS, Wanderlei TNG, Barbosa CS (2008) – Criadouros de Biomphalaria, temporários e permanentes, em of aquatic snail populations. Ex Parasitol 5:109 117 – Paraense WL (1972) Fauna planorbídica do Brasil. In: Lacaz CS, Baruzzi Jaboatão dos Guararapes, PE. Rev Soc Bras Med Trop 41:252 256 GR, Siqueira WJR (eds) Introdução à Geografia Médica do Brasil. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J (2006) Edgard Blucher & USP, São Paulo, pp 213–239 Schistosomiasis and water resources development: systematic re- Paraense WL (1975) The distribution of the molluscan vectors of schis- view, meta-analysis, and estimates of people at risk. Lancet Infect – tosomiasis in the Americas. Brasília Médica 11:11–14 Dis 6:25 41 Paraense WL (1981) Biomphalaria occidentalis sp.n. from South Telles HMS (1996) Distribuição de Biomphalaria straminea ao Sul da – America (: Basommatophora: ). Mem Inst Região Neotropical. Rev Saude Publica 30:341 349 Oswaldo Cruz 76:199–211 Telles HMS (2005) Distribuição geográfica das espécies dos caramujos Paraense WL (1984) Biomphalaria tenagophila guaibensis sp.n. from transmissores de Schistosoma mansoni no Estado de São Paulo. Rev southern Brazil and Uruguay (Pulmonata: Planorbidae). I. Soc Bras Med Trop 38:426–432 Morphology. Mem Inst Oswaldo Cruz 79:465–469 Thiengo SC, Fernandez MA (2008) Moluscos. In: Amaral RS, Thiengo Paraense WL (1988) (Clessin, 1883), planorbid SC, Pieri OS (eds) Vigilância e controle de moluscos de importância mollusc from South America. Mem Inst Oswaldo Cruz 83:1–12 epidemiológica. Diretrizes técnicas: Programa de Vigilância e Paraense WL (2008) Histórico do gênero Biomphalaria, morfologia e Controle da Esquistossomose (PCE). Fiocruz, Brasília, pp 13–36 sistemática morfológica. In: Carvalho OS, Coelho PMZ, Lenzi HL Vidigal THDA, Spatz L, Nunes ND, Simpson AJG, Carvalho OS, Dias- (eds) Schistosoma mansoni and Esquistossomose: uma visão Neto E (1998) Biomphalaria spp: identification of the intermediate multidisciplinar. Fiocruz, Rio de Janeiro, pp 285–308 snail hosts of Schistosoma mansoni by polymerase chain reaction Patz JA, Graczyk TK, Geller N, Vittor AY (2000) Effects of environmen- amplification and restriction enzyme digestion of the ribosomal tal change on emerging parasitic diseases. Int J Parasitol 30:1395– RNA gene intergenic spacer. Exp Parasitol 89:180–187 1405 Vitorino RR, Souza FPC, Costa AP, Faria-Júnior FC, Santana LA, Gomes Plam M, Jorgensen A, Kristensen TK, Madsen H (2008) Sympatric AP (2012) Esquistossomose mansônica: diagnóstico, tratamento, Biomphalaria species (Gastropoda: Planorbidae) in Lake Albert, epidemiologia, profilaxia e controle. Clinics 10:39–45