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Parasitology • Rev. Inst. Med. Trop. São Paulo 56 (3) • May-Jun 2014 • https://doi.org/10.1590/S0036-46652014000300010   copy

SPATIAL DISTRIBUTION OF LYMNAEIDAE (MOLLUSCA, BASOMMATOPHORA), INTERMEDIATE HOST OF Fasciola hepatica LINNAEUS, 1758 (TREMATODA, DIGENEA) IN BRAZIL

Distribuição espacial de Lymnaeidae (Mollusca, Basommatophora), hospedeiros intermediários de Fasciola hepatica Linnaeus, 1758 (Trematoda, Digenea) no Brasil

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstracts

Snails of the family Lymnaeidae act as intermediate hosts in the biological cycle of Fasciola hepatica, which is a biological agent of fasciolosis, a parasitic disease of medical importance for humans and animals. The present work aimed to update and map the spatial distribution of the intermediate host snails of F. hepatica in Brazil. Data on the distribution of lymnaeids species were compiled from the Collection of Medical Malacology (Fiocruz-CMM, CPqRR), Collection of Malacology (MZUSP), “SpeciesLink” (CRIA) network and through systematic surveys in the literature. Our maps of the distribution of lymnaeids show that Pseudosuccinea columella is the most common species and it is widespread in the South and Southeast with few records in the Midwest, North and Northeast regions. The distribution of the Galba viatrix, G. cubensis and G. truncatula showed a few records in the South and Southeast regions, they were not reported for the Midwest, North and Northeast. In addition, in the South region there are a few records for G. viatrix and one occurrence of Lymnaea rupestris. Our findings resulted in the first map of the spatial distribution of Lymnaeidae species in Brazil which might be useful to better understand the fasciolosis distribution and delineate priority areas for control interventions.

Lymnaeids; Fasciolosis; Spatial distribution; Snails; Brazil

Moluscos da família Lymnaeidae são hospedeiros intermediários no ciclo biológico de Fasciola hepatica, agente etiológico da fasciolose, doença parasitária de importância médica para humanos e animais. O presente trabalho teve como objetivo datar e mapear a distribuição espacial dos hospedeiros intermediários de F. hepatica no Brasil. Os dados de distribuição das espécies de limneídeos foram obtidos das Coleções de Malacologia Medica (Fiocruz-CMM, CPqRR) e de Malacologia do Museu de Zoologia da Universidade de São Paulo (MZUSP), rede “SpeciesLink” (CRIA) e através de pesquisas sistemáticas na literatura. Os mapas de distribuição dos limneideos mostram que Pseudosuccinea columella é a espécie mais comum e distribuída nas regiões Sul e Sudeste com poucos registros nas regiões Centro-Oeste, Norte e Nordeste. Além disso, na região Sul os registros para G. viatrix são escassos e existe apenas um único relato de ocorrência para L. rupestris. Os dados obtidos resultaram no primeiro mapa de distribuição espacial das espécies de Lymnaeidae no Brasil, informação básica e relevante para estruturação de políticas de controle da fasciolose humana e animal.

INTRODUCTION

Snails of the family Lymnaeidae are small Basommatophora hermaphrodites, approximately 10 mm long and 6 mm wide. The lymnaeids species is widely distributed around the tropical and subtropical areas of the Americas, Europe, Asia, Africa, and Oceania3636 Honer MR. Aspectos da epidemiologia da fasciolose. In: 1° Seminário Nacional sobre Parasitoses de Bovinos; 1979; Campo Grande. Anais. Brasília: EMBRAPA/CNPGC; 1979. p. 151-65. and inhabits natural (streams, ponds, swamps) or artificial (irrigation ditches, small dams, floodplain) types of water collections2323 Carvalho OS, Passos LKJ, Mendonça CLFG, Cardoso PCM, Caldeira RL. Moluscos de importância médica no Brasil. Belo Horizonte: Fiocruz/Centro de Pesquisas Rene Rachou; 2008..

The importance of the lymnaeids is due to the fact that they act as intermediate hosts in the biological cycle of the digenetic trematode Fasciola hepatica Linnaeus, 1758 (Trematoda, Digenea), biological agent of fasciolosis, which is a parasitic disease of medical importance for both humans and animals.

Based on an increasing number of human cases since 1980, MAS-COMA et al.5050 Mas-Coma S, Esteban JG, Bargues MD. Epidemiology of human fascioliasis: a review and proposed new classification. Bull World Health Organ. 1999;77:340-6. proposed that fasciolosis should be considered an important parasitic human disease rather than just a secondary zoonotic disease with an estimated number of infected people of more than 2.4 million people worldwide108108 World Health Organization. WHO. Triclabendazole and fascioliasis: a new drug to combat an age-old disease. Fact Sheets. 1998;191:1-4. Available from: http://www.who.ch/
http://www.who.ch/... . The economic losses caused by this disease include a significant impact on the livestock industry due to the high costs for therapeutic treatments in cattle, goat, and sheep breeding2424 Coelho LHL, Lima WS. Population dynamics of Lymnaea columella and its natural infection by Fasciola hepatica in the State of Minas Gerais, Brazil. J Helminthol. 2003;77:7-10.,2929 Dacal ARC, Costa HMD, Leite ACR. Susceptibilidade de Lymnaea (Pseudosuccinaea) columella (Say, 1817) exposta à infecção por miracídios de Fasciola hepatica (Linnaeus, 1758). Rev Inst Med Trop Sao Paulo. 1988;30:361-9.,4343 Luz E, Gazda CM, Yada RS. Fasciolose animal no Estado do Paraná: análise de dados. Arq Biol Tecnol. 1992;35:777-80.,4949 Mas-Coma S, Angles R, Strauss W, Esteban JG, Oviedo JA, Buchon P. Human fascioliasis in Bolivia: a general analysis and a critical review of existing data. Res Rev Parasitol. 1995;55:73-9.,8383 Sinclair KB. Pathogenesis of Fasciola and other liver - flukes. Heminthol Abstr. 1967;36:115-34.. SMOOKER et al.8484 Smooker PM, Hickford DE, Vaiano SA, Spithill TW. Isolation, cloning and expression of fatty acid binding proteins from Fasciola gigantica. Exp Parasitol. 1997;85:86-91. calculated a global cost of more than two billion dollars a year because of the infection.

In Brazil, the lymnaeids species already recorded are: Pseudosuccinea columella (Say, 1817), Galba viatrix d'Orbigny, 1835, Galba truncatula (Müeller, 1774), Galba cubensis Pfeiffer, 1839 and Lymnaea rupestris Paraense, 1982. Except for L. rupestris, the other species have proved to be susceptible to infection by F. hepatica. Regarding the identification of lymnaeids species, their systematics is confused and there are a lot of difficulties in identifying some species using only morphological characters2828 Correa AC, Escobar JS, Noya O, Velásquez LE, González-Ramírez C, Hurtrez-Boussès S, et al. Morphological and molecular characterization of Neotropic Lymnaeidae (Gastropoda: Lymnaeoidea), vectors of fasciolosis. Infect Genet Evol. 2011;11:1978-88.,7777 Samadi S, Roumégoux A, Bargues MD, Mas-Coma S, Yong M, Pontier JP. Morphological studies of Lymnaeidae snails from human fascioliasis endemic zone of Bolivia. J Molluscan Stud. 2000;66:31-44., so molecular markers are frequently necessary. Here, we used the taxonomy proposed by BAKER1313 Baker FC. The Natural History Survey of the Chicago Academy of Sciences. Chicago. Proccedings of the American Association of Museums; 1908;2:15-19. for the species P. columella.

The present work aimed to update and map the spatial distribution of the intermediate host snails of F. hepatica in Brazil.

MATERIAL AND METHODS

Malacological data: Data on the distribution of lymnaeids species were obtained from: i) Collection of Medical Malacology (Fiocruz-CMM) of the Laboratory of Medical Helminthology and Malacology, René Rachou Research Center (Fiocruz/MG); ii) Collection of Malacology of the Museum of Zoology of University of São Paulo (MZUSP); iii) “SpeciesLink” (CRIA) network (http://www.splink.org.br/), by using the keyword Lymnaeidae in the database search; iv) systematic surveys in scientific articles, gray literature, dissertations, theses, and communications, by using the combined keywords: Lymnaea/Galba/Pseudosuccinea/Lymnaeidae + occurrence + Brazil; Lymnaea/Galba/Pseudosuccinea/Lymnaeidae + distribution + Brazil; Lymnaea/Galba/Pseudosuccinea/Lymnaeidae + record + Brazil; Lymnaea/Galba/Pseudosuccinea/Lymnaeidae + collection + Brazil; Fasciola + occurrence + Brazil; Fasciola + distribution + Brazil; Fasciola + record + Brazil; Fasciolosis + occurrence + Brazil; Fasciolosis + distribution + Brazil and Fasciolosis + record + Brazil. According to the type of database (or sites), terms were used in English or Portuguese: Google scholar, Web of Knowledge, Scielo, PubMed, Periódicos Capes (Capes Journals) and Banco Digital de Teses e Dissertações (Theses and Dissertations Digital Database). The data collected had information relative to the occurrence of lymnaeids per state and municipalities of Brazilian regions and if the snails were found naturally infected by F. hepatica.

In the majority of the data used, the identification of the lymnaeids species was made using only morphological characters except when the data are from Fiocruz-CMM, where molecular markers were utilized to confirm the morphological identification. The molecular technique used was the polymerase chain reaction and restriction fragment length polymorphism (PCR-RFLP) targeted to the first and second internal transcribed spacers (ITS1 and ITS2) rDNA and to the mitochondrial 16S ribosomal gene (16S rDNAmt)1919 Cardoso PCM. Diferenciação molecular de moluscos do gênero Lymnaea (Gastropoda, Lymnaeidae) utilizando a PCR-RFLP e o estudo da variabilidade genética de L. columella pela RAPD. [dissertação]. Belo Horizonte: Centro de Pesquisas Rene Rachou, Fundação Oswaldo Cruz; 2004.,2222 Carvalho OS, Cardoso PCM, Lira PM, Rumi A, Roche A, Berne E, et al. The use of the polymerase chain reaction and restriction fragment length polymorphism technique associated with the classical morphology for characterization of Lymnaea columella, L. viatrix, and L. diaphana (Mollusca: Lymnaeidae). Mem Inst Oswaldo Cruz. 2004;99:503-7..

Data management and mapping: Data management, visualization and mapping were carried out in ArcGIS version 9.3 (ESRI; Redlands, CA, USA).

RESULTS

Reports on five species of Lymnaeidae were found in Brazil. Tables 1 and 2 summarize the distribution per locality of species in the five regions of Brazil (Fig. 1 and 2), South (Fig. 3), Southeast (Fig. 4), Midwest, North and Northeast regions (Fig. 5). In the “SpeciesLink” (CRIA) network, we found data relative to four collections: Collection of Molluscs of Museum of Science and Technology, PUCRS; Collection of Molluscs of National Institute of Research of Amazônia, INPA; Malacological Collection of Biological Science Department, DCBio/UFES and Collection of Malacology of Oswaldo Cruz Institute, Fiocruz-CMIOC. The information about the localities where the specimens occurred was not available from the Collection of Malacology of Oswaldo Cruz Institute, Fiocruz-CMIOC, because of this, we did not add these data to our results. The data from the Collection of Medical Malacology, Fiocruz-CMM, were already available to us.

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Table 1
Distribution of Pseudosuccinea columella per municipalities and regions of Brazil

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Table 2
Distribution of Galba viatrix, G. rupestris, G. cubensis, Lymnaea truncatula and Lymnaea sp. per municipalities and regions of Brazil

Fig. 1
Spatial distribution of Pseudosuccinea columella in Brazil.

Fig. 2
Spatial distribution of Galba viatrix, G. cubensis, G. truncatula, Lymnaea rupestris, and Lymnaea sp. in Brazil.

Fig. 3
Spatial distribution of Lymnaeidae in the South region of Brazil.

Fig. 4
Spatial distribution of Lymnaeidae in the Southeast region of Brazil.

Fig. 5
Spatial distribution of Lymnaeidae in the Midwest, North and Northeast regions of Brazil.

Lymnaeids snails were reported in 417 municipalities and one ecological reserve (Taim) of 16 states, which corresponds to 7.5% of all municipalities in Brazil. Pseudosuccinea columella was reported in 400 (95.7%) localities while G. viatrix in 10 (2.4%), G. cubensis in six (1.4%), G. truncatula in three (0.7%) and L. rupestris in one (0.2%). In 25 (6%) municipalities: Bom Jesus, Cambará do Sul, Erval Grande, Estrela, Ibirubá, Porto Alegre, São Borja, São Francisco de Paula, Selbach, Três Coroas, Vacaria and Viamão of Rio Grande do Sul State; Piracicaba, Presidente Prudente, São Paulo and Ubatuba of São Paulo State; Rio de Janeiro, Nova Friburgo, Teresópolis and Vassouras of Rio de Janeiro State; Ouro Branco and Careaçu of Minas Gerais State; Campos Novos/SC; Curitiba/PR and Belém/PA, it was not possible to accomplish a complete identification of the specimens collected. Occurrence of more than one species was reported in 13 municipalities (3.1%): Dom Pedrito, Pelotas and Santa Vitória do Palmar in the state of Rio Grande do Sul; Florianópolis (P. columella and G. viatrix) and Seara (L. rupestris, P. columella and G. viatrix) in the state of Santa Catarina; Teresópolis (P. columella; G. cubensis and G. truncatula), Nova Friburgo (P. columella and G. truncatula), Paraíba do Sul, Petrópolis, Rio de Janeiro and Três Rios (P. columella and G. cubensis) in the state of Rio de Janeiro; Belo Horizonte (P. columella, G. viatrix and G. cubensis) and Rio Acima (P. columella, G. viatrix and G. truncatula) in the state of Minas Gerais.

Specimens of P. columella and G. viatrix were reported in 403 localities (96.4%). P. columella was reported naturally infected with F. hepatica in 11 municipalities of the states of Rio Grande do Sul, São Paulo, Minas Gerais and Rio de Janeiro, G. viatrix was found naturally infected in three municipalities of Rio Grande do Sul while Lymnaea sp. was found in one municipality of Minas Gerais. In Dom Pedrito/RS, both species were found naturally infected.

DISCUSSION

Our study resulted in the first map of the spatial distribution of Lymnaeidae species, intermediate host snails of F. hepatica in Brazil. The presence of host snails could reflect the disease distribution, and these data are essential for describing the risk areas of fasciolosis since there is an increase of the association between the global number of human cases and the presence of the intermediate host snail5050 Mas-Coma S, Esteban JG, Bargues MD. Epidemiology of human fascioliasis: a review and proposed new classification. Bull World Health Organ. 1999;77:340-6..

PARAENSE6565 Paraense WL. Lymnaea viatrix and Lymnaea columella in the Neotropical Region: a distributional outline. Mem Inst Oswaldo Cruz. 1982b;77:181-8. showed that G. viatrix had few records in the South and P. columella was distributed mainly in the South and Southeast, where a high number of fasciolosis cases occurs3636 Honer MR. Aspectos da epidemiologia da fasciolose. In: 1° Seminário Nacional sobre Parasitoses de Bovinos; 1979; Campo Grande. Anais. Brasília: EMBRAPA/CNPGC; 1979. p. 151-65., with few records in the Midwest region. After that, the same author reported two new localities of P. columella for the states of Amazonas and Bahia6767 Paraense WL. Lymnaea columella: two new Brazilian localities in the states of Amazonas and Bahia. Mem Inst Oswaldo Cruz. 1986;8:121-3. in the North and Northeast respectively. This agrees with our study where we also reported a low presence of this species in these regions. Our final maps about spatial distribution of lymnaeids snails show that P. columella is the most common species and it is widespread in the South and Southeast with few records in the Midwest, North and Northeast regions. Galba viatrix is predominantly distributed in the South (eight records) with only two records for the Southeast region (Belo Horizonte and Rio Acima, Minas Gerais State). The distribution of G. viatrix, G. cubensis and G. truncatula comprises few records in Southeast and South regions. They were not reported for the Midwest, North and Northeast. For the South region, the species L. rupestris was only described and found in the Nova Teutônia district in Seara municipality at Santa Catarina State6464 Paraense WL. Lymnaea rupestris sp. n. from Southern Brazil (Pulmonata: Lymnaeidae). Mem Inst Oswaldo Cruz. 1982a;77:437-43..

Despite the few records showed by G. viatrix in our study, according to MATTOS & UENO5252 Mattos MJT, Ueno H. Suscetibilidade de Lymnaea viatrix e L. columella às infecções experimentais com Fasciola hepatica. Pesq Agropec Bras. 1989;24:615-22. this intermediate host is considered the most efficient species in the transmission of F. hepatica due to its high susceptibility when compared with P. columella5252 Mattos MJT, Ueno H. Suscetibilidade de Lymnaea viatrix e L. columella às infecções experimentais com Fasciola hepatica. Pesq Agropec Bras. 1989;24:615-22.. However, P. columella showed to be the most distributed species (Fig. 1; 95.7%) and is certainly the most important intermediate host in Brazil. This is probably due to its biological aspects, such as its high capacity for self-fertilization, favorable condition in dispersion and colonization of new habitats2020 Cardoso PCM, Caldeira RL, Lovato MB, Coelho PMZ, Berne MEA, Müller G, et al. Genetic variability of Brazilian populations of Lymnaea columella (Gastropoda: Lymnaeidae), an intermediate host of Fasciola hepatica (Trematoda: Digenea). Acta Trop. 2006;97:339-45.,3535 Gutiérrez A, Perera G, Yong M, Lin W. The effect of isolation on the life-history traits of Pseudosuccinea columella (Pulmonata: Lymnaeidae). Mem Inst Oswaldo Cruz. 2001;96:577-81.. Pseudosuccinea columella is commonly found in most human or animal fasciolosis outbreaks while the occurrence of G. viatrix is, currently, restricted to the state of Rio Grande do Sul2424 Coelho LHL, Lima WS. Population dynamics of Lymnaea columella and its natural infection by Fasciola hepatica in the State of Minas Gerais, Brazil. J Helminthol. 2003;77:7-10.,3333 Gonzales JC, Sanchez VM, Thome JW, Gonçalves PC, Oliveira CMB. Lymnaea columella, hospedeiro intermediário de Fasciola hepatica L. 1758, no Rio Grande do Sul, Brasil. Arq Fac Vet Rio Grande do Sul. 1974;2:37-40.,6363 Oliveira SM, Fuji TU, Sposito Filha E, Martins AMCRPF. Ocorrência de Lymnaea columella Say, 1817 infectada naturalmente por Fasciola hepatica (Linnaeus, 1758), no vale do Ribeira, São Paulo, Brasil. Arq Inst Biol (São Paulo). 2002;69:29-37.,7676 Rezende HEB, Araujo JLB, Gomes PAC, Nuernberg S, Neto MP, Oliveira GP et al. Notas sobre duas espécies de Lymnaea Lamark, 1799, hospedeiros intermediários da Fasciola hepatica no estado do Rio de Janeiro. (Mollusca, Gastropoda, Basommatophora, Lymnaeidae). Arq Univ Fed Rural. 1973;3:21-3.,101101 Ueta MT. Ocorrência de infecção natural de Fasciola hepatica Linnaeus, 1758 em Lymnaea columella Say, 1817 no vale do Paraíba, SP, Brasil. Rev Saude Publica. 1980;14:230-3. and in Minas Gerais2222 Carvalho OS, Cardoso PCM, Lira PM, Rumi A, Roche A, Berne E, et al. The use of the polymerase chain reaction and restriction fragment length polymorphism technique associated with the classical morphology for characterization of Lymnaea columella, L. viatrix, and L. diaphana (Mollusca: Lymnaeidae). Mem Inst Oswaldo Cruz. 2004;99:503-7..

In relation to the others susceptible species, G. cubensis occurs only in the Southeast, mainly in Rio de Janeiro State1919 Cardoso PCM. Diferenciação molecular de moluscos do gênero Lymnaea (Gastropoda, Lymnaeidae) utilizando a PCR-RFLP e o estudo da variabilidade genética de L. columella pela RAPD. [dissertação]. Belo Horizonte: Centro de Pesquisas Rene Rachou, Fundação Oswaldo Cruz; 2004.,6060 Nuernberg S. Estudos experimentais com Lymnaea cubensis Pfeiffer, 1839 (Mollusca, Gastropoda, Basommatophora, Lymnaeaidae) como hospedeiro intermediário de Fasciola hepatica L. 1758 (Trematoda, Fasciolidae), no Estado do Rio de Janeiro. [tese]. Rio de Janeiro: Universidade Federal Rural do Rio de Janeiro; 1978.,7676 Rezende HEB, Araujo JLB, Gomes PAC, Nuernberg S, Neto MP, Oliveira GP et al. Notas sobre duas espécies de Lymnaea Lamark, 1799, hospedeiros intermediários da Fasciola hepatica no estado do Rio de Janeiro. (Mollusca, Gastropoda, Basommatophora, Lymnaeidae). Arq Univ Fed Rural. 1973;3:21-3.. There was a gap of 30 years in its record and until now its presence in other regions was not reported. Galba truncatula is also susceptible to F. hepatica, however with few records (0.7%) it has never been found naturally infected in Brazil. Lymnaea rupestris was only described and found in one locality and there is no information about its susceptibility. Due to these facts, the role in the transmission of fasciolosis of the species above mentioned remains unknown.

In the present study, it was possible to observe the occurrence of P. columella in several localities of the South (four municipalities) and Southeast (seven municipalities) and of G. viatrix in the South (three municipalities) naturally infected by F. hepatica (Table 1 and 2). In the South region, the presence of extensive endemic areas of fasciolosis is frequent, while in the Southeast and Midwest regions there are only small endemic areas4141 Lima WS, Soares LRM, Barçante TA, Guimarães MP, Barçante JMP. Occurrence of Fasciola hepatica (Linnaeus, 1758) infection in Brazilian cattle of Minas Gerais, Brazil. Rev Bras Parasitol Vet. 2009;18:27-30.. Some environmental and climatic factors in the South region provide favorable habitats for the intermediate host snails of F. hepatica, such as low elevation (where there are numerous rice fields), clay soil, humid areas, and a temperate climate. These habitats, as shown by UENO et al.9898 Ueno H, Gutierres VC, Mattos MJT, Müller G. Fascioliasis problems in ruminants in Rio Grande do Sul, Brazil. Vet Parasitol. 1982;11:185-91., contribute to the maintenance of the snails' life cycle in this region.

Despite the great efforts made by research groups, some important issues related to the nature and precision of the presence of lymnaeid species in Brazil need to be considered when interpreting our findings. The complete distribution of intermediate host snails of F. hepatica in Brazil remains unknown, especially due to the large areas that need to be surveyed mainly in the North and Midwest regions. Other restraining factors include the insufficient number of researchers involved in the taxonomy area, which may cause difficulties in identifying the snails at a species level due to the confusing taxonomic situation of the Lymnaeidae family. It was confirmed by our study that in several localities (25 municipalities; 6%) the specific identification was not possible to be done. The identification of specimens is important since knowing the species that act as intermediate hosts in a particular area, we can define priority strategies regarding intermediate hosts biology to control fasciolosis. In Careaçu, MG, the occurrence of naturally-infected specimens without specific identification was reported (Table 2).

Another important point concerns the validity of the species identification used from the literature data and malacological collections due to systematics confusion of lymnaeids snails. This identification is essential in order to justify the distribution of lymnaeid species in Brazil. Regarding L. rupestris and P. columella, there is no problem because these two species can be easily identified using a set of reliable morphological characters and the literature data can be used with a reasonable confidence. However, this is not the case regarding the three other remaining species, G. viatrix, G. cubensis and G. truncatula, because these small species cannot be separated morphologically and only molecular markers allow a clear separation1414 Bargues MD, Artigas P, Mera y Sierra RL, Pointier JP, Mas-Coma S. Characterisation of Lymnaea cubensis, L. viatrix and L. neotropica n. sp., the main vectors of Fasciola hepatica in Latin America, by analysis of their ribosomal and mitochondrial DNA. Ann Trop Med Parasitol. 2007;101:621-41.,2727 Correa AC, Escobar JS, Durand P, Renaud F, David P, Jarne P, et al. Bridging gaps in the molecular phylogeny of the Lymnaeidae (Gastropoda: Pulmonata), vectors of Fascioliasis. BMC Evol Biol. 2010;10:1-12.,2828 Correa AC, Escobar JS, Noya O, Velásquez LE, González-Ramírez C, Hurtrez-Boussès S, et al. Morphological and molecular characterization of Neotropic Lymnaeidae (Gastropoda: Lymnaeoidea), vectors of fasciolosis. Infect Genet Evol. 2011;11:1978-88.,5656 Meunier C, Tirard C, Hurtrez-Boussès S, Durand P, Bargues MD, Mas-Coma S, et al. Lack of molluscan host diversity and the transmission of an emerging parasitic disease in Bolivia. Mol Ecol. 2001;10:1333-40.,7373 Pointier JP, González-Salas C, Gutiérrez A, Arenas JA, Bargues MD, et al. Anatomical studies of sibling species within neotropical lymnaeids, snail intermediate hosts of fascioliasis. Mem Inst Oswaldo Cruz. 2006;101:431-5.,7777 Samadi S, Roumégoux A, Bargues MD, Mas-Coma S, Yong M, Pontier JP. Morphological studies of Lymnaeidae snails from human fascioliasis endemic zone of Bolivia. J Molluscan Stud. 2000;66:31-44.. In our literature search we identified only 19 localities where the specific identification might be a concern (10 localities with G. viatrix, six localities with G. cubensis and three localities with G. truncatula). Only in the occurrence of G. cubensis for Belo Horizonte, MG1919 Cardoso PCM. Diferenciação molecular de moluscos do gênero Lymnaea (Gastropoda, Lymnaeidae) utilizando a PCR-RFLP e o estudo da variabilidade genética de L. columella pela RAPD. [dissertação]. Belo Horizonte: Centro de Pesquisas Rene Rachou, Fundação Oswaldo Cruz; 2004., G. truncatula for Rio Acima, MG2222 Carvalho OS, Cardoso PCM, Lira PM, Rumi A, Roche A, Berne E, et al. The use of the polymerase chain reaction and restriction fragment length polymorphism technique associated with the classical morphology for characterization of Lymnaea columella, L. viatrix, and L. diaphana (Mollusca: Lymnaeidae). Mem Inst Oswaldo Cruz. 2004;99:503-7. and the data from Fiocruz-CMM have the authors already carried out molecular identification.

Studies on the lymnaeid fauna should be increased all over Brazil, mainly where the information is scarce or nonexistent, with the objective to learn more about the spatial distribution of the intermediate host snail of F. hepatica. The methodology used and the intermediate host snail final maps could be useful in identifying priority areas for control interventions of fasciolosis, so that limited resources could be allocated most effectively.

ACKNOWLEDGEMENTS

We would like to thank the Health Sciences Library “Prof. Zigman Brener” of the Research Center René Rachou and the assistant Nuzia Pereira dos Santos for allowing access to scientific information through the availability of the required articles. We thank Dr. Luiz Ricardo Simone, Zoology Museum of University of São Paulo for allowing access to the data from the Malacological Collection of Zoology Museum of University of São Paulo. We thank Dr. Jean Pierre Pointier, University of Perpignan, France, for their important suggestions on the manuscript. We also thank José Geraldo Amorim, Laboratory of Medical Helminthology and Malacology, CPqRR, Fiocruz/MG for collecting snails of the Collection Fiocruz-CMM. This work was partially sponsored by the Fapemig (Process APQ-01633-10), CNPq (Process 150386/2012-5), CPqRR - Programa de Excelência em Pesquisa, PROEP/CPqRR (Process 401968/2012-0) and CNPq - Doutorado Sanduiche no Exterior, SWE/CNPq (Process 245926/2012-7).

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Publication Dates

  • Publication in this collection
    May-Jun 2014

History

  • Received
    19 Dec 2012
  • Accepted
    17 Sept 2013
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