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Spatial Distribution and Seasonality of Biomphalaria Spp Parasitology Research (2018) 117:1495–1502 https://doi.org/10.1007/s00436-018-5810-1 ORIGINAL PAPER Spatial distribution and seasonality of Biomphalaria 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 species of Schistosoma mansoni Sambon, 1907 in Brazil occur in the state of Maranhão: Biomphalaria glabrata (Say, 1818) and Biomphalaria straminea (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 Animal, 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 Schistosoma mansoni 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). Biomphalaria tenagophila (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,
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