Freshwater snails and Schistosomiasis mansoni in the state of Rio de Janeiro, Brazil: IV - Sul Fluminense Mesoregion

EPIDEMIOLOGY

Freshwater snails and Schistosomiasis mansoni in the state of Rio de Janeiro, Brazil: IV - Sul Fluminense Mesoregion

Silvana C Thiengo¹; Aline C Mattos; M Fernanda Boaventura; Monica A Fernandez

Departamento de Malacologia, Instituto Oswaldo Cruz-Fiocruz, Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brasil

ABSTRACT

In this paper, the forth of a series dealing with the survey of freshwater gastropods of the state of Rio de Janeiro, the results of collections carried out in the Sul Fluminense Mesoregion from 2000 to 2002 are presented and revealed the occurrence of 18 species: Antillorbis nordestensis; Biomphalaria glabrata; Biomphalaria peregrina; Biomphalaria straminea; Biomphalaria tenagophila; Drepanotrema anatinum; Drepanotrema cimex; Drepanotrema lucidum; Ferrissia sp.; Gundlachia ticaga; Gundlachia sp.; Heleobia sp.; Lymnaea columella; Melanoides tuberculatus; Physa acuta; Physa marmorata; Pomacea sordida and Pomacea sp. As to the snail hosts of Schistosoma mansoni the most frequent species was B. tenagophila, found in all municipalities surveyed, except Parati. Besides new records the present study extends the distribution of B. peregrina and B. straminea in the state. No specimens were found harbouring larval forms of S. mansoni although different kinds of cercariae had been observed. An account about the current schistosomiasis transmission sites in this Mesoregion is presented as well.

Key words: freshwater snails - schistosomiasis mansoni - cercariae - Rio de Janeiro - Brazil

Aiming to elaborate a Chart of planorbids of the state of Rio de Janeiro collections have been done by the authors since 1997. During the last two years, from March, 2000 to May, 2002, collecting was done in the following municipalities of the Sul Fluminense Mesoregion: Barra Mansa, Itatiaia, Pinheiral, Piraí, Porto Real, Quatis, Resende, Rio Claro, and Volta Redonda (Vale do Paraíba Fluminense Microregion); Barra do Piraí, Rio das Flores, and Valença (Barra do Piraí Microregion); Angra dos Reis and Parati (Baía da Ilha Grande Microregion).

The freshwater snail species listed include specimens collected by the authors as well as those in the Collection of the Department of Malacology of Instituto Oswaldo Cruz. The distribution of the snail species of medical and veterinary importance, various kinds of cercariae and the number of schistosomiasis cases reported to this region during the last 18 years are also presented.

MATERIALS AND METHODS

We have adopted the Brazilian Institute of Geography and Statistic (IBGE 1995) procedures in dividing the state of Rio de Janeiro into six Mesoregions (Baixadas, Metropolitana, Centro Fluminense, Sul Fluminense, Norte Fluminense, and Noroeste Fluminense) and the Center of Information and Data of Rio de Janeiro (CIDE 2001) for the new municipalities. The Sul Fluminense Mesoregion is 7931 km², constituting 18.1% of the state.

The molluscs were collected from different suitable snail habitats from all 48 districts of the 14 municipalities surveyed. Since at least three different habitats were investigated in each of the districts, an average of 167 samples was obtained. Live snails were kept at the laboratory for a month in aquaria containing dechlorinated tap water and, at the bottom, a thin layer of a 2:1 mixture of screened soil and ground oyster shells as a source of mineral nutrients. Snails were fed on fresh lettuce leaves. In the meantime all specimens were exposed to artificial light at five-day intervals to determine possible infection with trematode larvae. Cercariae were fixed in 70% ethanol, stained with chloridric carmine, mounted in Canada balsam and subsequently identified according to Schell (1970).

The ten larger specimens of each sample were preserved in Railliet-Henry's fluid after relaxation in a 0.05% nembutal solution and two of them were dissected under stereomicroscope for identification.

Samples of taxonomic importance were deposited at the Malacological and Helminthological Collections of Instituto Oswaldo Cruz.

The cases of schistosomiasis reported from 1985 to 2003 were obtained from the National Health Foundation (Funasa).

RESULTS

Table I shows the localities where the 18 molluscan species were found: Antillorbis nordestensis (Lucena, 1954); Biomphalaria glabrata (Say, 1818); Biomphalaria peregrina (Orbigny, 1835); Biomphalaria straminea (Dunker, 1848); Biomphalaria tenagophila (Orbigny, 1835); Drepanotrema anatinum (Orbigny, 1835); Drepanotrema cimex (Moricand, 1839); Drepanotrema lucidum (Pfeiffer, 1839); Ferrissia sp.; Gundlachia ticaga (Marcus & Marcus, 1962); Gundlachia sp.; Heleobia sp.; Lymnaea columella Say, 1817; Melanoides tuberculatus (Müller, 1774); Physa acuta Draparnaud, 1805; Physa marmorata Guilding, 1828; Pomacea sp., and Pomacea sordida (Swainson, 1823).

The distribution of the intermediate hosts of Schistosoma mansoni Sambon, 1907 as well as that of L. columella the main intermediate host of Fasciola hepatica (Linné) in Brazil is shown in the Figure.

Map showing the distribution of the species of medical and veterinary importance. () Biomphalaria glabrata; () Biomphalaria straminea; () Biomphalaria tenagophila; () Biomphalaria peregrina; () Lymnaea columella

The highest species richness occurred in Piraí (12 species), Resende (12), and Valença (12). On the other hand, in Porto Real only five species were found.

Specimens of P. marmorata were found in all municipalities and among the planorbid species, the most frequent was B. tenagophila, observed in 13 municipalities.

Although many different kinds of cercariae had been observed (Table II), no specimens were found infected with S. mansoni or F. hepatica. Xiphidiocercariae (including Ubiquita cercaria and Ornatae cercaria) were the most frequent type of trematode larvae, followed by Echinostome cercariae. The major diversity of cercariae was found in Barra Mansa, in the following species: B. tenagophila, D. cimex, L. columella, and P. marmorata. As shown in the Table II, out of 122 infected snails, there were found harbouring Xiphidiocercariae (51.6%), Strigid cercaria (26.2%), Echinostome cercaria (13.1%) and Brevifurca-apharingeata-clinostomatoide cercariae (4.9%).

Even though no specific parasitological surveys have been performed by Funasa in the Sul Fluminense Meso-region, cases of schistosomiasis were detected in Angra dos Reis, Barra do Piraí, Barra Mansa, Itatiaia, Parati, Pinheiral, Piraí, Porto Real, Quatis, Resense, Rio Claro, Valença, and Volta Redonda (Table III).

DISCUSSION

The present study extended the geographical distribution of B. tenagophila and B. straminea, natural vectors of schistosomiasis in Brazil. B. straminea was previously recorded in 22 municipalities in the state of Rio de Janeiro (Paraense 1986, Grault et al. 1995, Thiengo et al. 1998, 2001, 2002a, b) and the records for Angra dos Reis, Barra do Piraí, Pinheiral, Piraí, Resende, Rio das Flores, and Volta Redonda are new. Up to now it had only been found in Barra Mansa according to Grault et al. (1995).

Althought no specimens of B. glabrata have been found in the present study, Paraense (1975) reported that snail vector in Barra do Piraí. However, caution is needed in attributing the disappearance of this species, considered the most important host of S. mansoni in Brazil, due to its high susceptibilitity to infection.

The distributional pattern of B. peregrina, considered a potential vector by Paraense and Corrêa (1973), has been extended to include Barra do Piraí, Itatiaia, Quatis, and Resende.

In relation to the non-vector planorbid species, D. lucidum was the most common, followed by D. anatinum, D. cimex, and A. nordestensis. In the previously studied Mesoregions, the most frequent species were D. anatinum in the Metropolitana and Centro Fluminense Mesoregions (Thiengo et al. 2001, 2002a) and D. cimex in the Baixadas Mesoregion (Thiengo et al. 2002b). The distribution of A. nordestensis, previously known in 24 municipalities in the state (Thiengo et al. 1998, Santos et al. 1999, Thiengo et al. 2001, 2002a, b), is now extended to include Angra dos Reis, Parati, Resende, and Valença.

Of the remaining Pulmonata species, P. marmorata was found most frequently (all municipalities; 39 districts), followed by L. columella (all municipalities except Porto Real; 30 districts) and P. acuta (9 municipalities; 17 districts). According to Paraense and Pointier (2003), P. acuta proved indistinguishable, in shell and anatomy, from topotypic Physa cubensis Pfeiffer, 1839, pointing to the synonymy of the two nominal species under the older name. Thus, the distribution of P. acuta in the state was now extended to 41 municipalities.

The Afro-Asian thiarid M. tuberculatus was found in the Vale do Paraíba Fluminense (3 municipalities) and Baía da Ilha Grande Microregions (1 municipality). Recently, Fernandez et al. (2003) reported the wide distribution of this species in Brazil and argued about its employment as competitor of snail intermediate hosts of S. mansoni in Brazil and Caribe. Possible environmental impacts caused by M. tuberculatus high dense populations that have been observed at different natural breeding sites in Brazil are pointed out as well.

Concerning the Prosobranchia, hydrobiid species were found only in the Baía da Ilha Grande Microregion. Specimens of Pomacea sp., collected from six municipalities, resembled those reported by Thiengo et al. (2002a) in Centro Fluminense and Baixadas Mesoregions. Further morphological studies are being undertaken on samples from those regions, aiming to identify them.

Among the ancylids G. ticaga was the most frequently found species, occurring in all municipalities surveyed, except Porto Real. The same was observed in the previously studied Mesoregions, e.g., Metropolitana, Centro Fluminense, and Baixadas (Thiengo et al. 2001, 2002a, b).

Although the number of positive cases must be seen as underestimated information, because of the limitation of logistic resources available to Funasa, the results of the coproscopical and malacological surveys carried out showed cases of schistosomiasis in Barra Mansa and pointed out B. tenagophila as the snail intermediate host. Even though the transmission has been reducing after intervention carried out since 1985 by the local health authorities, this municipality is still recognized as a low transmission site in the state.

The distribution of L. columella overlaps the occurrence of fascioliasis foci in this Mesoregion (Serra-Freire et al. 1995) as well as the first report of a human case in the state, e. g., in Volta Redonda (Pile et al. 2000).

With regard to other trematode, the xiphidiocercariae was the most frequently larval type found in the molluscs, corroborating Thiengo et al. (2002a,b).

ACKNOWLEDGEMENTS

To Luiz Carlos Pina (Funasa/RJ) for informing the number of cases of schistosomiasis and to Dr Sonia Barbosa dos Santos for identification of the ancylid species.

Received 14 November 2003

Accepted 22 March 2004

Financial support: CNPq, Faperj, Fiocruz

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Publication Dates

• Publication in this collection
  19 July 2004
• Date of issue
  May 2004

History

• Received
  14 Nov 2003
• Accepted
  22 Mar 2004