Freshwater gastropods of the Baixada Maranhense Microregion, an endemic area for schistosomiasis in the State of Maranhão, Brazil: I - qualitative study

Selma Patricia Diniz Cantanhede Monica Ammon Fernandez Aline Carvalho de Mattos Lângia Colli Montresor Nêuton Silva-Souza Silvana Carvalho Thiengo About the authors

Abstract

Introduction:

The Baixada Maranhense Microregion currently has the highest prevalence of schistosomiasis in the State of Maranhão, likely because this parasitosis is characterized as an occupational disease, and increased contact with water increases the risk of infection by Schistosoma mansoni. This paper reports the results of the first comprehensive freshwater malacological survey performed in the Baixada Maranhense Microregion.

Methods:

Freshwater mollusks were collected from the twenty-one municipalities of the Baixada Maranhense Microregion and from Bacurituba and Cajapió and were evaluated for infection by trematodes.

Results:

A total of 9,129 mollusks were collected (sixteen species), which included the first records of six species in the State of Maranhão: Gundlachia radiata, G. ticaga, Hebetancylus moricandi, Plesiophysa guadeloupensis, Pomacea bridgesii diffusa and Omalonyx sp. Biomphalaria glabrata was found in five municipalities, whereas B. straminea was found in nine. Biomphalaria glabrata and B. straminea were observed in syntopy in Pinheiro and São Bento. Of the 990 specimens of B. glabrata and the 2,109 specimens of B. straminea that were exposed to and/or analyzed for the presence of larval trematodes, only a single specimen of B. glabrata (0.1%) from São Bento shed S. mansoni. Other larval trematodes were first observed in mollusks from the State of Maranhão.

Conclusions:

These results indicate that the study area is epidemiologically important due to the presence of two natural vectors of schistosomiasis and the active transmission of schistosomiasis, which was confirmed in the infected specimen that was collected in this study.

Freshwater snails; Schistosoma mansoni ; Vectors; Baixada Maranhense Microregion; Brazil; Cercaria


INTRODUCTION

Of the snail-transmitted diseases, schistosomiasis is undoubtedly the most important to public health. In Brazil, schistosomiasis occurs in 19 states, which represents a large endemic area along the coast from the State of Maranhão to Espírito Santo and Minas Gerais. Schistosomiasis also occurs in isolated foci within the States of Piauí, Pará, Goiás, Distrito Federal, São Paulo, Rio de Janeiro, Paraná, Santa Catarina and Rio Grande do Sul11. Coura JR, Amaral RS. Epidemiological and control aspects of schistosomiasis in Brazilian endemic areas. Mem Inst Oswaldo Cruz 2004; 99 (Suppl I):13-19.,22. Ministério da Saúde. Sistema de Informação do Programa de Vigilância e Controle da Esquistossomose (SIPCE). Brasília: Ministério da Saúde; 2012. [March, 2013] Available at http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sinan/pce/cnv/pce.def/.
http://tabnet.datasus.gov.br/cgi/deftoht...
. The disease has been recorded in Maranhão since 192033. Cutrim RNM, Chieffi PP, Moraes JC. Schistosomiasis mansoni in the “Baixada Ocidental Maranhense”, state of Maranhão, Brazil: cross-sectional studies performed in 1987 and 1993. Rev Inst Med Trop São Paulo 1998; 40:165-171., its distribution is endemic in 20 of 217 municipalities and 29 municipalities have reported foci44. Ministério da Saúde. Sistema Nacional de Vigilância em Saúde: Relatório de Situação: Maranhão. 5th. ed. Brasília: Ministério da Saúde. Secretaria de Vigilância em Saúde; 2011.. The two snail vectors Biomphalaria glabrata (Say, 1818) and Biomphalaria straminea (Dunker, 1848) have been reported in 30 and 40 municipalities, respectively55. Carvalho OS, Amaral RS, Dutra LV, Scholte RGC, Guerra MAM. Distribuição espacial de Biomphalaria glabrata, B. straminea e B. tenagophila, hospedeiros intermediários do Schistosoma mansoni no Brasil. In: Carvalho OS, Coelho PMZ, Lenzi H, editors. Schistosoma mansoni & Esquistossomose: uma visão multidisciplinar. Rio de Janeiro: Editora Fiocruz; 2008. p. 393-418..

The Baixada Maranhense Microregion, which is one of the seven ecological regions of Maranhão, represents the main group of lacustrine basins in the northeast and is a complex ecological system that consists of temporary, shallow, marginal and permanent lakes that are commonly known as flooded grasslands. Despite being an interesting ecological system, the Baixada Maranhense Microregion is not protected from environmental damage, such as extensive-breeding buffalo farming, irrigation projects and dam construction66. Costa-Neto JP, Barbieri R, Ibañez MSR, Cavalcante PRS, Piorski NM. Limnologia de três ecossistemas aquáticos característicos da Baixada Maranhense. Bol Lab Hidrobiol 2002; 14/15:19-38.. Currently, the Baixada Maranhense Microregion shows the highest prevalence of schistosomiasis in the state44. Ministério da Saúde. Sistema Nacional de Vigilância em Saúde: Relatório de Situação: Maranhão. 5th. ed. Brasília: Ministério da Saúde. Secretaria de Vigilância em Saúde; 2011.. This parasitosis is characterized as an occupational disease because activities such as fishing, hunting and farming, which result in increased contact with water, also increase the risk of infection by Schistosoma mansoni (Sambon, 1907)77. Ferreira LA, Lima FL, Anjos MR, Costa JML. Forma tumoral encefálica esquistossomótica: apresentação de um caso tratado cirurgicamente. Rev Soc Bras Med Trop 1998; 31:89-93..

Therefore, this paper reports the results of the first comprehensive freshwater malacological survey performed in the Baixada Maranhense Microregion. This study investigated the distribution of snail vectors of S. mansoni and contribute to a better understanding of schistosomiasis transmission within this Microregion.

METHODS

The Baixada Maranhense Microregion is 17,909km2 and corresponds to approximately 5.4% of the total area of Maranhão, which includes 21 municipalities88. Instituto Brasileiro de Geografia e Estatística (IBGE). Divisão Territorial do Brasil e Limites Territoriais [Internet]. Rio de Janeiro: IBGE [Cited 2008 July 1]. Available at: http//:www.ibge.gov.br/.
http//www.ibge.gov.br/...
. Freshwater mollusks were collected from each of the municipalities (Anajatuba, Arari, Bela Vista do Maranhão, Cajari, Conceição do Lago Açu, Igarapé do Meio, Matinha, Monção, Olinda Nova, Palmeirândia, Pedro do Rosário, Penalva, Peri-Mirim, Pinheiro, Presidente Sarney, Santa Helena, São Bento, São João Batista, São Vicente Férrer, Viana and Vitória do Mearim) and from Bacurituba and Cajapió, which are two neighboring municipalities with geographic characteristics that are similar to those of the Baixada Maranhense Microregion. The specimens were obtained from different biotopes (streams, rivers, marsh areas, drainage and sewage ditches, ponds, flooded areas and irrigation canals) in November 2011 and in March, July and October 2012. Four collectors performed 10-minute searches in each biotope, and all collection sites were georeferenced.

In the Laboratório de Malacologia of Instituto Oswaldo Cruz/FIOCRUZ, Rio de Janeiro-RJ, specimens were placed in aquaria containing dechlorinated water, substrate and food (fresh lettuce leaves). To search for larvae, the samples were processed following the protocol of Mattos et al.99. Mattos AC, Boaventura MFF, Fernandez MA, Thiengo SC. Larval trematodes in freshwater gastropods from Mato Grosso, Brazil: diversity and host-parasites relationships. Biota Neotrop 2013; 13:1-5.. Except for Omalonyx sp., all of the snails were individually exposed to artificial light to determine if they were infected with S. mansoni larvae or any other trematode of medical or veterinary importance, and the trematode larvae were identified using key specifics according to Schell1010. Schell S. How to Know the Trematodes. Dubuque: WMC Brown Co. Publishers; 1970.. The mollusks were examined using a stereomicroscope, and negative mollusks were crushed to confirm the absence of larval trematodes1111. Fernandez MA, Thiengo SC, Amaral RS. Técnicas malacológicas. In: Amaral RS, Thiengo SC, Pieri OS, editors. Vigilância e Controle de Moluscos de moluscos de Importância Médica: Diretrizes Técnicas. Brasilia: Editora do Ministério da Saúde; 2008. p. 43-70.. Live cercarial stages were obtained by exposure under an incandescent light, and other larval stages were determined during crushing or anatomical dissections. Ten specimens of each sample were anesthetized in Hypnol 0.05% solution for five hours, killed by hot water (70°C) and fixed in Railliet-Henry solution for morphological analysis1111. Fernandez MA, Thiengo SC, Amaral RS. Técnicas malacológicas. In: Amaral RS, Thiengo SC, Pieri OS, editors. Vigilância e Controle de Moluscos de moluscos de Importância Médica: Diretrizes Técnicas. Brasilia: Editora do Ministério da Saúde; 2008. p. 43-70.. Mollusk samples were deposited at the Coleção de Moluscos of Instituto Oswaldo Cruz (CMIOC).

RESULTS

Mollusks were confirmed in 176 of the 230 biotopes that were surveyed (Table 1), including S. mansoni vectors (Figure 1). Some species were recorded for the first time, as shown in Figure 2.

TABLE 1
- Families, species and municipalities where mollusks were found in the Baixada Maranhense Microregion, Maranhão, Brazil.

FIGURE 1
- Map of the State of Maranhão and the Baixada Maranhense Microregion (left). Baixada Maranhense Microregion (right) showing the distribution Schistosoma mansoni vectors: Δ Biomphalaria glabrata;  Biomphalaria straminea and ▀ B. glabrata and B. straminea.

FIGURE 2
- Map of the State of Maranhão and the Baixada Maranhense Microregion (left). Baixada Maranhense Microregion (right) showing the first record of species: ▾ Gundlachia radiata; ? Gundlachia ticaga; ∆ Hebetancylus moricandi; ● Plesiophysa guadeloupensis; ○ Pomacea bridgesii diffusa; ◊ Omalonyx sp.; ◊ Omalonyx sp. and H. moricandi; ? Omalonyx sp. and P. guadeloupensis.

Five gastropod families were obtained: Ampullariidae, Ancylidae, Planorbidae, Physidae and Succineidae. A total of 9,129 individuals were collected and identified, including 990 specimens of Biomphalaria glabrata (Say, 1818); 122 specimens of Biomphalaria schrammi (Crosse, 1864); 2,106 specimens of Biomphalaria straminea (Dunker, 1848); 275 specimens of Drepanotrema anatinum (d'Orbigny, 1835); 56 specimens of Drepanotrema cimex (Moricand, 1839); 273 specimens of Drepanotrema depressissimum (Moricand, 1839); 1,811 specimens of Drepanotrema lucidum (Pfeiffer, 1839); 9 specimens of Gundlachia radiata (Guilding, 1828); 9 specimens of Gundlachia ticaga (Marcus & Marcus, 1962); 17 specimens of Hebetancylus moricandi (d'Orbigny, 1837); 1,047 specimens of Physa marmorata Guilding, 1828; 31 specimens of Plesiophysa guadeloupensis (Crosse & Fischer in Mazé, 1883); 1,424 specimens of Pomacea maculata Perry, 1810 and 12 specimens of Pomacea bridgesii diffusa (Blume, 1957). In addition, shells or juveniles of Ancylidae (24 shells), Biomphalaria sp. (863 shells) and Omalonyx sp. (57 juveniles) were obtained.

The highest diversity of mollusks species was observed in the municipality of São Bento, where 12 species were reported. In contrast, the municipality of Cajari had the lowest species diversity (only P. maculata).

Of the species of medical and veterinary importance, B. glabrata was identified in five municipalities, whereas B. straminea was found in nine. These species were observed in syntopy in two biotopes of Pinheiro and in four biotopes of São Bento. Of the 990 specimens of B. glabrata and 2,109 specimens of B. straminea that were exposed and/or analyzed for the presence of larval trematodes, only a single specimen of B. glabrata (0.1%) from the municipality of São Bento shed S. mansoni cercariae.

Other types of cercariae were shedded from six different mollusk species (Table 2): Armatae cercaria, Brevifurcate-apharingeate-cercaria, Echinostome cercaria, Monostome cercaria, Ornatae cercaria, Strigea cercaria, Ubiquita cercaria and Vivax cercaria. In addition, the metacercariae of Echinostomatidae were observed in B. glabrata specimens from São Bento, Pinheiro and São Vicente Férrer, whereas one specimen of P. maculata from São Vicente Férrer was infected with Echinostomatidae rediae.

TABLE 2
- Types of cercariae and the municipalities where they were found in the Baixada Maranhense Microregion, Maranhão, Brazil.

Echinostome cercaria were the most frequent cercariae found in the mollusks, and the highest percentage of infected snails was recorded in São João Batista (14.2%), followed by Conceição do Lago Açu (8.8%). Drepanotrema lucidum was infected with the highest diversity of cercariae (five different types).

Of the fifteen species that were examined, nine contained no larval trematodes: B. schrammi, Biomphalaria sp., D. anatinum, D. cimex, G. radiata, G. ticaga, H. moricandi, P. guadeloupensis and P. bridgesii diffusa.

DISCUSSION

The Baixada Maranhense Microregion is epidemiologically important because of the presence of two natural vectors of schistosomiasis and the occurrence of active transmission of schistosomiasis, which was confirmed based on the infected specimen that was collected. According to the information available at the Schistosomiasis Information System (SISPCE)22. Ministério da Saúde. Sistema de Informação do Programa de Vigilância e Controle da Esquistossomose (SIPCE). Brasília: Ministério da Saúde; 2012. [March, 2013] Available at http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sinan/pce/cnv/pce.def/.
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, the Baixada Maranhense Microregion shows a higher prevalence of schistosomiasis than Peri Mirim (7.2% in 2010; 4.07% in 2011) and São Bento (6.12% in 2010; 6.48% in 2011; and 6.13% in 2012).

This study revealed an extended distribution of two species of medical importance: B. glabrata in Bacurituba and B. straminea in Conceição do Lago Açu, Igarapé do Meio, Monção, Pedro do Rosário, Penalva and Vitória do Mearim.

Within the Baixada Maranhense Microregion, B. glabrata has reportedly been found in the municipalities of Anajatuba, Palmeirândia, Peri Mirim, Pinheiro, São Bento, São João Batista, São Vicente Férrer and Viana. Previous reports have found B. straminea in Arari, Cajapió, Matinha, Palmeirândia, Peri-Mirim, Pinheiro, Santa Helena, São Bento, São João Batista, São Vicente Férrer and Viana1212. Paraense WL. A survey of planorbid molluscs in the Amazonian region of Brazil. Mem Inst Oswaldo Cruz 1983; 78:343-361.. Our study confirms the existing data regarding the occurrence of B. glabrata in Peri Mirim, Pinheiro, São Bento and São Vicente and B. straminea in Arari, Pinheiro and São Bento.

The present study confirmed the occurrence of the non-vector planorbid species B. schrammi and D. depressissimum in São Bento and D. lucidum in Arari, which coincides with the results of a previous study that was performed in the Amazon Region by Paraense1212. Paraense WL. A survey of planorbid molluscs in the Amazonian region of Brazil. Mem Inst Oswaldo Cruz 1983; 78:343-361.. The most common species of Drepanotrema that were observed in this study included D. anatinum and D. lucidum. Similarly, in the freshwater malacological survey studies that were performed in the state of Rio de Janeiro, D. anatinum was the most frequently observed in the four Mesoregions (Metropolitana, Centro Fluminense, Norte and Noroeste Fluminense), whereas D. lucidum was the most frequently observed in the Sul Fluminense Mesoregion1313. Thiengo SC, Fernandez MA, Boaventura MF, Grault CE, Silva HFR, Mattos, AC, et al. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: I - Metropolitan Mesoregion. Mem Inst Oswaldo Cruz 2001; 96 (Suppl I): 177-184.1616. Thiengo SC, Mattos AC, Santos SB, Fernandez MA. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: VI – Noroeste Fluminense Mesoregion. Mem Inst Oswaldo Cruz 2006; 101 (suppl I): 239-245..

The diversity of cercarial types shed from D. lucidum was also observed in other studies; Echinostome cercaria was the most frequent type1717. Boaventura MF, Thiengo SC, Fernandez MA. Gastrópodes límnicos hospedeiros intermediários de trematódeos digenéticos no Brasil. In: Santos SB, Pimenta A, Thiengo SC, Fernandez MA, Absalão RS, editors. Tópicos em Malacologia: Ecos do XVIII Encontro Brasileiro de Malacologia. Rio de Janeiro: Sociedade Brasileira de Malacologia; 2011. p. 327-337.. Drepanotrema lucidum from the state of Mato Grosso presented the largest variety of larval trematode forms, and Echinostome cercaria were present in most of the gastropod families that were studied in all of the Brazilian regions1717. Boaventura MF, Thiengo SC, Fernandez MA. Gastrópodes límnicos hospedeiros intermediários de trematódeos digenéticos no Brasil. In: Santos SB, Pimenta A, Thiengo SC, Fernandez MA, Absalão RS, editors. Tópicos em Malacologia: Ecos do XVIII Encontro Brasileiro de Malacologia. Rio de Janeiro: Sociedade Brasileira de Malacologia; 2011. p. 327-337.. Echinostomatidae is the most common trematode family that parasitizes freshwater gastropods in Brazil99. Mattos AC, Boaventura MFF, Fernandez MA, Thiengo SC. Larval trematodes in freshwater gastropods from Mato Grosso, Brazil: diversity and host-parasites relationships. Biota Neotrop 2013; 13:1-5.. The biological interactions between snails and trematodes found in Maranhão state extends the list of cercariae in mollusks from Brazil that was recently related by Pinto and Melo1818. Pinto HA, Melo AL. checklist of larval trematodes (Platyhelminthes) in molluscs from Brazil. Zootaxa 2013; 3666:449-475..

Brevifurcate-apharingeate-cercaria can cause cercarial dermatitis1919. Hoeffler DF. Cercarial dermatitis, its etiology, epidemiology and clinical aspects. Arch Environ Health 1974; 29:225-229.,2020. Hanning GW, Leedom WS. Schistosome Dermatites from Pomacea paludosa (Say) (Prosobranchia: Pilidae). The Nautilus 1978; 92:105-106.; these types of cercaria were found in specimens of B. glabrata from São Bento and P. maculata from Anajatuba. Some trematode larvae of Schistosomatidae can cause cercarial dermatitis, which is an effective skin immune response caused by cercarial penetration. The apparent emergence of cercarial dermatitis should be understood as the spread of disease to a new area (e.g., Chile and the United Kingdom) or the increased contact between people and larval trematodes2121. Horák P, Kolárová L. Snails, waterfowl and cercarial dermatitis. Freshwater Biol 2011; 56:779-790.. Although not recorded in Brazil, the intermediate mollusk hosts are widely distributed in the country. These trematodes have also been found in birds2222. Pinto HA, Mati VLT, Melo AL. Dermatite cercariana por esquistossomatídeos de aves: é possível a ocorrência de casos no Brasil? Rev Patol Trop 2012; 41:1-14..

This study provides the first record of the ampullariid P. bridgesii diffusa in the state of Maranhão. Currently, this species, which is native to the Amazon Basin, is found in Brazil, Bolivia and Peru2323. Cowie RH, Thiengo SC. The apple snails of the Americas (Mollusca: Gastropoda: Ampullariidae: Asolene, Felipponea, Marisa, Pomacea, Pomella): a nomenclatural and type catalog. Malacologia 2003, 45:41-100.. The Baixada Maranhense Microregion is situated in the transition zone between the Amazon and the Northeast 2424. Conceição MVS, Moreira JF, Farias Filho MS. O espaço natural da Baixada Maranhense. In: Farias Filho MS, editor. O espaço geográfico da Baixada Maranhense, São Luís, MA: JK Gráfica Editora; 2012. p.19., which is more precisely located in the Amazonia Maranhense, where P. bridgesii diffusa was recorded in a contiguous area that covers three municipalities. The wide distribution of the congeneric species P. maculata within the region and the large number of specimens that were collected confirm that the species has a wide range of morphological, behavioral and physiological adaptations that have possibly contributed to the high diversity and distribution of those mollusks in a large population density2525. Hayes KA, Cowie RH, Thiengo SC. A global phylogeny of apple snails: Gondwanan origin, generic relationships, and the influence of outgroup choice (Caenogastropoda: Ampullariidae). Biol J Linn Soc 2009; 98:61-76.. Pornacea maculata is distributed from the western region of Brazil, the border of Paraguay, to the south and north of the Amazon Basin, and it is an important component of the biodiversity of freshwater mollusks of the Pantanal2626. Hayes KA, Cowie RH, Thiengo SC, Strong EE. Comparing apples to apples: clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda). Zool J Linn Soc 2012; 166:723-753..

Ancylidae that were found in this study are widely distributed in South America2727. Santos SB. Estado atual do conhecimento dos ancilídeos na América do Sul (Mollusca: Gastropoda: Pulmonata: Basommatophora). Rev Biol Trop 2003; 51:191-223.. Furthermore, our results are similar to those of previous studies that reported G. radiata and G. ticaga as the most common species. Indeed, in the state of Rio de Janeiro, G. ticaga was the most common species[13-16;28,29], whereas, in the state of Goiás3030. Thiengo SC, Santos SB, Fernandez MA. Malacofauna límnica da área de influência do lago da usina hidrelétrica de Serra da Mesa, Goiás, Brasil. I. Estudo qualitativo. Rev Bras Zool 2005; 22:867-874., G. radiata and G. ticaga were among the species that were found.

Three species of the genus Omalonyx have been recorded in Brazil: Omalonyx matheroni (Pontiez & Michaud, 1835) from Amazonas, Minas Gerais, Pará, Paraná, Pernambuco, Rio de Janeiro and São Paulo3131. Arruda JO, Pereira D, Bergonci PEA, Santos CP, Mansur MCD. Novos registros de Omalonyx matheroni (Potiez & Michaud, 1835) (Mollusca, Gastropoda, Succineidae) para os Estados de São Paulo e Paraná, Brasil. Biotemas 2009; 22:187-190.; and O. brasiliensis (Simroth, 1896) and O. convexus (Heynemann, 1868) from the State of Rio Grande do Sul3232. Arruda JO, Thomé JW. Synonymization of Neohyalimax Simroth, 1896, and Omalonyx d'Orbigny, 1837, with a redescription of Omalonyx brasiliensis (Simroth, 1896) (Gastropoda: Succineidae). The Nautilus 2008; 2:94-98.,3333. Arruda JO, Tomé JW. Biological aspects of Omalonyx convexus (Mollusca, Gastropoda, Succineidae) from the Rio Grande do Sul State, Brazil. Revista Biotemas 2011; 24:95-101.. This report is the first account of Omalonyx sp. in Maranhão State.

Similarly, this paper reports the first record of P. guadeloupensis in Maranhão. In Brazil, P. guadeloupensis was previously reported in the States of Bahia, Espírito Santo, Minas Gerais, Paraíba, Pernambuco, Rio de Janeiro, Rio Grande do Norte and Sergipe3434. Fernandez MA, Thiengo SC, Paraense WL. Primeiro registro de Plesiophysa guadeloupensis (“Fischer” Mazé) no Estado do Rio de Janeiro, Brasil. Rev Bras Zool 2006; 23:883-885.. In the present study, the specimens were found in two neighboring municipalities, Pedro do Rosário (locality of Três Palmeiras) and Santa Helena (locality of Mangabeira).

This paper is the first extensive malacological survey of freshwater mollusks in the state of Maranhão. Additional malacological surveys with the intention of obtaining quantitative data to contribute to future studies, such as the monitoring of snail vectors of schistosomiasis and the gain of a comprehensive knowledge of freshwater mollusks from that region, are underway. Additionally, further molecular studies on the larval forms of trematodes that infect mollusks will be performed to aid in their identification.

Acknowledgments

We thank the Secretaria de Estado da Saúde do Maranhão for valuable support during the field work, Dra. Sonia B. Santos for the identification of ancylids and Paula T. Bermudez for the illustrations.

REFERENCES

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    Thiengo SC, Fernandez MA, Boaventura MF, Grault CE, Silva HFR, Mattos, AC, et al. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: I - Metropolitan Mesoregion. Mem Inst Oswaldo Cruz 2001; 96 (Suppl I): 177-184.
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    Thiengo SC, Mattos AC, Boaventura MF, Loureiro MS, Santos SB, Fernandez MA. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: V - Norte Fluminense Mesoregion. Mem Inst Oswaldo Cruz 2004a; 99 (suppl I):99-103.
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    Thiengo SC, Mattos AC, Santos SB, Fernandez MA. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: VI – Noroeste Fluminense Mesoregion. Mem Inst Oswaldo Cruz 2006; 101 (suppl I): 239-245.
  • 17
    Boaventura MF, Thiengo SC, Fernandez MA. Gastrópodes límnicos hospedeiros intermediários de trematódeos digenéticos no Brasil. In: Santos SB, Pimenta A, Thiengo SC, Fernandez MA, Absalão RS, editors. Tópicos em Malacologia: Ecos do XVIII Encontro Brasileiro de Malacologia. Rio de Janeiro: Sociedade Brasileira de Malacologia; 2011. p. 327-337.
  • 18
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  • 19
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  • 20
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  • 21
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  • 22
    Pinto HA, Mati VLT, Melo AL. Dermatite cercariana por esquistossomatídeos de aves: é possível a ocorrência de casos no Brasil? Rev Patol Trop 2012; 41:1-14.
  • 23
    Cowie RH, Thiengo SC. The apple snails of the Americas (Mollusca: Gastropoda: Ampullariidae: Asolene, Felipponea, Marisa, Pomacea, Pomella): a nomenclatural and type catalog. Malacologia 2003, 45:41-100.
  • 24
    Conceição MVS, Moreira JF, Farias Filho MS. O espaço natural da Baixada Maranhense. In: Farias Filho MS, editor. O espaço geográfico da Baixada Maranhense, São Luís, MA: JK Gráfica Editora; 2012. p.19.
  • 25
    Hayes KA, Cowie RH, Thiengo SC. A global phylogeny of apple snails: Gondwanan origin, generic relationships, and the influence of outgroup choice (Caenogastropoda: Ampullariidae). Biol J Linn Soc 2009; 98:61-76.
  • 26
    Hayes KA, Cowie RH, Thiengo SC, Strong EE. Comparing apples to apples: clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda). Zool J Linn Soc 2012; 166:723-753.
  • 27
    Santos SB. Estado atual do conhecimento dos ancilídeos na América do Sul (Mollusca: Gastropoda: Pulmonata: Basommatophora). Rev Biol Trop 2003; 51:191-223.
  • 28
    Thiengo SC, Fernandez MA, Boaventura MF, Magalhães MG, Santos SB. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: III - Baixadas Mesoregion. Mem Inst Oswaldo Cruz 2002b; 97 (Suppl I):43-46.
  • 29
    Thiengo SC, Mattos AC, Boaventura MF, Fernandez MA. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: IV - Sul Fluminense Mesoregion. Mem Inst Oswaldo Cruz 2004b; 99:275-280.
  • 30
    Thiengo SC, Santos SB, Fernandez MA. Malacofauna límnica da área de influência do lago da usina hidrelétrica de Serra da Mesa, Goiás, Brasil. I. Estudo qualitativo. Rev Bras Zool 2005; 22:867-874.
  • 31
    Arruda JO, Pereira D, Bergonci PEA, Santos CP, Mansur MCD. Novos registros de Omalonyx matheroni (Potiez & Michaud, 1835) (Mollusca, Gastropoda, Succineidae) para os Estados de São Paulo e Paraná, Brasil. Biotemas 2009; 22:187-190.
  • 32
    Arruda JO, Thomé JW. Synonymization of Neohyalimax Simroth, 1896, and Omalonyx d'Orbigny, 1837, with a redescription of Omalonyx brasiliensis (Simroth, 1896) (Gastropoda: Succineidae). The Nautilus 2008; 2:94-98.
  • 33
    Arruda JO, Tomé JW. Biological aspects of Omalonyx convexus (Mollusca, Gastropoda, Succineidae) from the Rio Grande do Sul State, Brazil. Revista Biotemas 2011; 24:95-101.
  • 34
    Fernandez MA, Thiengo SC, Paraense WL. Primeiro registro de Plesiophysa guadeloupensis (“Fischer” Mazé) no Estado do Rio de Janeiro, Brasil. Rev Bras Zool 2006; 23:883-885.

  • Conflict of Interest: The authors declare that there is no conflict of interest.
  • Financial Support: Fundação Oswaldo Cruz, CAPES - Coordenação de Aperfeiçoamento de Pessoal e Nível Superior, Secretaria de Estado da Saúde do Maranhão and Universidade Estadual do Maranhão.

Publication Dates

  • Publication in this collection
    Jan-Feb 2014

History

  • Received
    29 Oct 2013
  • Accepted
    3 Feb 2014
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