Geographical distribution of intermediate hosts of Schistosoma mansoni in the states of Paraná, Minas Gerais, Bahia, Pernambuco and Rio Grande do Norte, Brazil, 2012-2014**This project was funded by the Department of Health Surveillance of the Brazilian Ministry of Health (National Health Foundation/Ministry of Health: Term of Cooperation No. 173/2010), René Rachou Institute/Oswaldo Cruz Foundation/Belo Horizonte, MG, and Oswaldo Cruz Institute/Oswaldo Cruz Foundation/Rio de Janeiro, RJ. The project was carried out in accordance with article 14 of Law No. 5,197, dated 3 January 1967 ('Law of Fauna'), which provides for the granting to scientists belonging to scientific institutions, a special license for collecting material for scientific purposes.

Omar dos Santos Carvalho Cristiane Lafetá Furtado de Mendonça Jeann Marie da Rocha Marcelino Liana Konovaloff Jannotti Passos Monica Ammon Fernandez Raquel de Souza Leal Roberta Lima Caldeira Ronaldo Guilherme Carvalho Scholte Eduardo Hage Carmo Silvia Gonçalves Mesquita Silvana Carvalho Thiengo About the authors

Abstract

Objective:

to describe the geographical distribution of intermediate hosts of Schistosoma mansoni in five Brazilian states.

Methods:

this was a descriptive cross-sectional study; municipalities were selected in the states of Paraná (78), Minas Gerais (120), Bahia (82), Pernambuco (51) , and Rio Grande do Norte (98), for the period 2012 to 2014; these municipalities were chosen because they did not have current records of the presence of snails vectores de S. mansoni. The molluscs were captured and taxonomically identified and examined for S. mansoni cercariae.

Results:

the work was carried out in 427 municipalities (99.5% of the 429 selected); the presence of mollusks was registered in 300 (70.2%) municipalities; Biomphalaria glabrata were found in 62 (21%) municipalities, B. straminea in 181 (60%), B. tenagophila in three (1%); B. glabrata/B. straminea association was found in 53 municipalities (18%) and B. glabrata/B. tenagophila association in one (0.3%) municipality.

Conclusion:

B. glabrata, B. straminea and B. tenagophila distribution records obtained in this study are consistent with previously known distribution.

Keywords:
Schistosomiasis; Biomphalaria; Disease Vectors; Geographic Mapping

Introduction

Schistosomiasis mansoni is a parasitic infectious disease11. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: Diretrizes Técnicas. 4. ed. Brasília: Ministério da Saúde, 2014. the etiological agent of which is the Schistosoma mansoni trematode. It is endemic in approximately 49 countries of the Americas, Caribbean and Africa. In Brasil, from 1975 to 2012, the percentage of schistosomiasis positivity ranged from 4.5 to 23.3%, while the highest prevalences are found in the Northeast and Southeast regions of the country. From 1988 to 2013 the hospitalization rate ranged from 2.5 to 0.08/ 100,000 inhabitants and the mortality rate in the period from 1987 to 2012 ranged from 0.5 to 0.2/100,000 inhabitants.11. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: Diretrizes Técnicas. 4. ed. Brasília: Ministério da Saúde, 2014.

The invertebrate hosts are planorbidae mollusks of the Biomphalaria genus. Among the 11 species and one subspecies of mollusks of this genus recognized in Brazil, only Biomphalaria glabrata, Biomphalaria tenagophila and Biomphalaria straminea have been found naturally infected with S. mansoni so far. The most important intermediate host is B. glabrata, because of its high susceptibility to S. mansoni and wide distribution. In Brazil, its occurrence is almost always associated with the presence of schistosomiasis mansoni.22. Paraense WL. Distribuição dos caramujos no Brasil. In: Reis FA, Faria I, Katz N, organizadores. Modernos Conhecimentos sobre Esquistossomose Mansônica. Belo Horizonte: Academia Mineira de Medicina; 1986; v. 1, p.117-128.

Biomphalaria tenagophila has spread along the coastal strip from the south of the state of Bahia to Rio Grande do Sul. In the states of Minas Gerais, São Paulo, Paraná and Rio Grande do Sul, the species is moving west. B. tenagophila has epidemiological importance in the Paraíba Valley in São Paulo state.

Biomphalaria straminea has the broadest geographical distribution and is present in almost all Brazilian river basins. Due to its extensive distribution, B. straminea is the species best adapted to all varieties of climates and ecological conditions of the country. This species has importance in the epidemiology of schistosomiasis in some states of Northeast Brazil. The lack of malacological research in Brazil explains the shortage of data on the geographical distribution of these species of mollusks.22. Paraense WL. Distribuição dos caramujos no Brasil. In: Reis FA, Faria I, Katz N, organizadores. Modernos Conhecimentos sobre Esquistossomose Mansônica. Belo Horizonte: Academia Mineira de Medicina; 1986; v. 1, p.117-128.

A further three species, Biomphalaria peregrina, Biomphalaria amazonica and Biomphalaria cousini, and a hybrid of the latter two were experimentally infected and are considered potential hosts of the parasite.33. Corrêa LR, Paraense WL. Susceptibility of Biomphalaria amazonica to infection with two strains of Schistosoma mansoni. Rev Inst Med Trop São Paulo. 1971;13:387-90.

4. Paraense WL, Corrêa LR. Susceptibility of Biomphalaria peregrina from Brazil and Ecuador to two strains of Schistosoma mansoni. Rev Inst Med Trop São Paulo. 1973; 15:127-30.
-55. Teodoro TM, Jannotti-Passos LK, Carvalho OS, Caldeira RL. Occurrence of Biomphalaria cousini (Mollusca: Gastropoda) in Brazil and its susceptibility to Schistosoma mansoni (Platyhelminths: Trematoda). Mol Phyl Evol. 2010; 57:144-51.

In 2008, the Ministry of Health, following the recommendation of the Technical Advisory Committee of Schistosomiasis Program, redefined the data on the geographical distribution of S. mansoni mollusk hosts of in the country’s states, focusing on transmission as topic of relevance to the Schistosomiasis Surveillance and Control Program.

The geographical distribution of S. mansoni intermediate hosts by Brazilian municipalities has been progressively updated, on the basis of new records of the presence of the three host species.66. Carvalho OS, Scholte RGC, Amaral RS. Distribuição Espacial de Biomphalaria glabrata, B. straminea e B. tenagophila Hospedeiros Intermediários de Schistosoma mansoni no Brasil. In: Carvalho OS, Coelho PMZ, Lenzi HL, (Org.). Schistosoma mansoni e Esquistossomose: uma visão multidisciplinar. 2008. 1 ed. Rio de Janeiro: Fiocruz; 2008; v. 1, p. 529-46.

7. Piza JT, Ramos AS. Os focos autóctones de esquistossomose no Estado de São Paulo. Arq Hig Saúde Pública. 1960; 25:261-71.

8. Schlemper Junior BR, Ferreira Neto JA, Thiago PTS, Bressan C, Amarante AR. Distribuição geográfica de Planorbídeos em Santa Catarina, Brasil. Rev Soc Bras Med Trop. 1996; 29:411-18.

9. Paraense WL. Planorbídeos hospedeiros intermediários do Schistosoma mansoni. In: Cunha AS, organizadores. Esquistossomose mansoni. São Paulo: Universidade de São Paulo; 1970.

10. Paraense WL. Fauna planorbídica do Brasil. In: Lacaz CS, Baruzzi RG, Siqueira Junior W, organizadores. Introdução à geografia médica do Brasil. São Paulo: Edgard Blücher, Universidade de São Paulo; 1972.

11. Paraense WL. The distribution of the molluscan vectors of schistosomiasis in the Americas. Brasília Médica. 1975a;11:11-14.

12. Carvalho OS, Nunes IM, Caldeira RL. First report of Biomphalaria glabrata in the state of Rio Grande do Sul, Brazil. Mem Inst Oswaldo Cruz. 1998; 93:39-40.

13. Paraense WL. The schistosome vectors in the Americas. Mem Inst Oswaldo Cruz. 2001; 96(suppl):7-16.

14. Souza CP, Caldeira RL, Drummond SC, Melo AL, Guimarães CT, Delza MS, Carvalho OS. Geographical Distribution of Biomphalaria Snails in the State of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz. 2001; 96:293-302.

15. Teles HMS, Pereira PAC, Richinitti LMZ. Distribuição de Biomphalaria (Gastropoda, Planorbidade) nos Estados do Rio Grande do Sul e Santa Catarina, Brasil. Rev Saúde Pública de São Paulo. 1991; 25:350-2.

16. Teles HMS. Distribuição geográfica das espécies dos caramujos transmissores de Schistosoma mansoni no Estado de São Paulo, Brasil. Rev Soc Bras de Med Trop. 2005; 38:426-32.

17. Thiengo SC, Fernandez MA, Boaventura MFF, Stortti MA. A survey of freshwater gastropods in the Serrana Mesoregion of the state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 1998; 93(supl I):233-4.

18. Thiengo SC, Fernandez MA, Boaventura MFF, Grault CE, Silva HF, Mattos AC, Santos SB. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: I - Metropolitan mesoregion. Mem Inst Oswaldo Cruz. 2001;96:177-84.

19. Thiengo SC, Fernandez MA, Boaventura MFF, Magalhães MG, Santos SB. Freshwater snails and Schistosomiasis mansoni in the state of Rio de Janeiro, Brazil: III - Baixadas Mesoregion. Mem Inst Oswaldo Cruz. 2002a; 97:43-6.

20. Thiengo SC, Fernandez MA, Boaventura MFF, Silva HF, Mattos AC, Santos SB. Freshwater snails and Schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: II - Centro Fluminense Mesoregion. Mem Inst Oswaldo Cruz. 2002b(5);97:621-6.

21. 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. 2004; 99:275-80.

22. 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(supl. I):239-45.

23. 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; 22:867-74.
-2424. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Vigilância e controle de moluscos de importância epidemiológica. Diretrizes técnicas: programa de Vigilância e Controle da Esquistossomose (PCE). Brasília: Ministério da Saúde; 2008. Records of B. glabrata occurrence are delimited by the 0 53'S (Quatipuru, PA), 29 51'S (Esteio, RS), 53 44'S (Toledo, PR) parallels and the coastline; B. straminea is delimited by the 02º54'S and 31º00'S parallels, longitude 44º43'W and the coastline; and B. tenagophila is delimited by the quadrant between the 10º12°'S and 33º41'S parallels, longitude 57º05'W and the coastline.99. Paraense WL. Planorbídeos hospedeiros intermediários do Schistosoma mansoni. In: Cunha AS, organizadores. Esquistossomose mansoni. São Paulo: Universidade de São Paulo; 1970.,1212. Carvalho OS, Nunes IM, Caldeira RL. First report of Biomphalaria glabrata in the state of Rio Grande do Sul, Brazil. Mem Inst Oswaldo Cruz. 1998; 93:39-40.

The objective of this study was to describe the geographical distribution of intermediate hosts of S. mansoni in five Brazilian states.

Methods

This is a descriptive ecological study, carried out in the period from September 2012 to October 2014. Quantitative and qualitative techniques (morphological identification) were used to survey intermediate hosts of S. mansoni, as well as information previously recorded on the collection of mollusks kept at the Oswaldo Cruz Institute/Oswaldo Cruz Foundation, Rio de Janeiro, RJ (Fiocruz/CMIOC). The study coverage area comprised 429 municipalities in states of Paraná (78), Minas Gerais (120), Bahia (82) Pernambuco (51) and Rio Grande do Norte (98). These municipalities were chosen because they did not have current records of the presence of intermediate hosts of S. mansoni. The samples were collected by a team composed of researchers and health professionals from the municipalities, previously trained at each state’s reference laboratory.

Three water collections were selected by municipality, with priority being given to places where local populations have greater contact with water and where there are favorable conditions for the occurrence of planorbidae.1818. Thiengo SC, Fernandez MA, Boaventura MFF, Grault CE, Silva HF, Mattos AC, Santos SB. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: I - Metropolitan mesoregion. Mem Inst Oswaldo Cruz. 2001;96:177-84.

Mollusks were collected at different water collection points. To achieve this, a perforated metal ladle (with holes around 2mm) or a riddle fixed to a handle approximately 1m in length were used. Submerged vegetation on the banks was scraped as was the bottom of the water collection points, in order to collect an adequate amount of specimens. There is no defined sampling technique for this kind of survey. All the specimens found were stored in plastic containers, labeled and taken to the laboratory.

The data on the geographic coordinates of all the places surveyed were obtained by means of GPS receivers and recorded using the decimal system.

The examination of S. mansoni larvae in the mollusks specimens2424. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Vigilância e controle de moluscos de importância epidemiológica. Diretrizes técnicas: programa de Vigilância e Controle da Esquistossomose (PCE). Brasília: Ministério da Saúde; 2008. was performed at the Helminthology and Medical Malacology Laboratory of the René Rachou Institute/Oswaldo Cruz Foundation (IRR/Fiocruz) and at the Malacology Laboratory of the Oswaldo Cruz Institute/Fiocruz (IOC/Fiocruz). We used the technique of light stimulus or crushing between glass plates to detect the presence or absence of trematodes. Morphological identification was carried out at these two laboratories and also at the Laboratory of the Paraná State Health Department.

The dissection of the mollusks was done according to the Deslandes protocol;2525. Deslandes N. Técnica de dissecação e exame de planorbídeos. Rev Serv Espec Saúde Pública. 1950;4:371-82. specific identification was performed according to the protocols established by Paraense,2626. Paraense WL. Estado atual da sistemática dos planorbídeos brasileiros. Arq Mus Nac. 1975b;55:105-28. based on morphological characters. Molecular identification2727. Vidigal T, Caldeira RL, Simpson AJG, Carvalho OS. Further studies on the molecular systematic of Biomphalaria snails from Brazil. Mem Inst Oswaldo Cruz. 2000;95:57-66. was performed by the René Rachou Institute/Fiocruz Helminthology and Medical Malacology Laboratory, on at least one specimen from each catchment point in the states of Paraná, Minas Gerais and Pernambuco. The molecular profiles were compared to the standard profiles of the DNA extracted from snails tissue from the Medical Malacology Collection (Fiocruz/CMM).

Stata version 10.1 (Stata LP, College Station, TX, USA) was used for data analysis and the maps were drawn using ArcGIS software version 9.3 (Esri, Redlands, CA, USA).

The State Health Departments involved supported the study by making technical staff available for field work and also by providing transport to the collection sites. The formalization of their agreement was done by means of an official document.

The survey was conducted in accordance with Normative Instruction No. 141 of 19 December 2006, which regulates the environmental control and management of harmful synanthropic fauna.

Results

After checking with the state and municipal health authorities, the number of municipalities to be included was adjusted, since the state of Paraná had already done a survey in 172 municipalities. A further 93 municipalities were included in the other states, namely 52 in Minas Gerais, 6 in Bahia, 32 in Pernambuco and 3 in Rio Grande do Norte. In the latter state, it was not possible to perform collection in two municipalities (Grossos and Galinhos) due to the most severe drought in the last 100 years and consequent absence of environments propitious to freshwater mollusks.

Of the 429 municipalities selected for the study data were obtained from 427 municipalities (99.5%) (Table 1), mollusks of the Biomphalaria genus were found in 300 (70.2%). These snails were found in 120 municipalities in the state of Minas Gerais and 78 municipalities in the state of Paraná (Figure 1), these being in the country’s Southeast and Southern regions, and in 82 municipalities in the state of Bahia, 51 in Pernambuco and 98 in Rio Grande do Norte, these being in the country’s Northeast region (Figure 2). Data on 61 of these municipalities had already been already recorded as part of collection of mollusks kept at the Oswaldo Cruz Institute. The presence of B. glabrata was recorded in 62 municipalities, B. straminea in 181 and B. tenagophila in three municipalities. In 53 municipalities, B. glabrata was associated with B. straminea; and in one municipality, B. glabrata was found associated with B. tenagophila (Table 1).

Table 1
- Result of the capture of Biomphalaria glabrata, Biomphalaria tenagophila and Biomphalaria straminea in Paraná, Minas Gerais, Bahia, Pernambuco and Rio Grande do Norte, December 2012 - June 2014

Figure 1
- Map of Brazil highlighting the states surveyed (A) and distribution of Schistosoma mansoni intermediate hosts in Minas Gerais (B) and Paraná (C), December 2012 - June 2014

Figure 2
- Distribution of Schistosoma mansoni intermediate hosts in Bahia (A) Pernambuco (B) and Rio Grande do Norte (C), December 2012 - June 2014

Mollusks were infected with S. mansoni in three (1%) of the 300 municipalities where mollusks were present, all three of them being in the state of Bahia: Itororó (eight), Arataca (one) and Teolândia (nine). The results of collection per municipality, in the five states surveyed (Figure 1A), are presented below:

Minas Gerais (Figure 1B)

Biomphalaria glabrata (33): Aricanduva, Cachoeira de Pajeú, Capelinha, Carmésia, Catas Altas, Crisólita, Cristiano Otoni, Diogo de Vasconcelos, Divisópolis, Frei Gaspar, Itaverava, Jeceaba, Lamim, Mato Verde, Monte Formoso, Ouro Verde de Minas, Palmópolis, Piranga, Presidente Bernardes, Queluzita, Rio do Prado, Rio Espera, Rubim, Santa Helena de Minas, Santana dos Montes, Santo Antônio do Itambé, São Brás do Suaçuí, São Gonçalo do Rio Preto, Senhora de Oliveira, Senhora do Porto, Senhora dos Remédios, Serra Azul de Minas and Serro.

Biomphalaria tenagophila (1): Santa Rita de Jacutinga.

Biomphalaria straminea (28): Acaiaca, Águas Formosas, Almenara, Araçuaí, Bandeira, Barra Longa, Barroso, Berilo, Bertópolis, Carbonita, Coronel Murta, Francisco Badaró, Franciscópolis, Fronteira dos Vales, Ingaí, Itutinga, Jenipapo de Minas, José Gonçalves de Minas, Lagoa Dourada, Leme do Prado, Monjolos, Nanuque, Santa Maria do Salto, Senador Modestino Gonçalves, Turmalina, Veredinha, Virgem da Lapa and Umburatiba.

B. glabrata/B. straminea (16): Alto Rio Doce, Alvorada de Minas, Ataléia, Carlos Chagas, Couto Magalhães de Minas, Felício dos Santos, Felisburgo, Itamarandiba, Itaobim, Jordânia, Ladainha, Pavão, Ponto dos Volantes, Santo Antônio do Jacinto, São Gonçalo do Rio Abaixo and Setubinha.

B. glabrata/B. tenagophila (1): Rio Pomba.

Negative municipalities (41): Angelândia, Carrancas, Casa Grande, Catuji, Conceição da Barra de Minas, Congonhas, Congonhas do Norte, Datas, Desterro de Entre Rios, Desterro do Melo, Dores de Campos, Entre Rios de Minas, Gouvea, Ibertioga, Ibituruna, Itaipé, Madre de Deus de Minas, Mercês, Morro do Pilar, Nazareno, Novo Oriente de Minas, Padre Paraíso, Paiva, Passa Tempo, Piedade do Rio Grande, Poté, Prados, Presidente Kubitschek, Raposos, Resende Costa, Ressaquinha, Ritápolis, Santa Barbara do Tugurio, Santa Cruz de Minas, Santana do Garambéu, Santo Antônio do Rio Abaixo, Santo Hipólito, São Tiago, Serra dos Aimorés, Serranos and Tiradentes.

Paraná (Figure 1C).

Biomphalaria tenagophila (2): Araucária and Contenda.

Biomphalaria straminea (16): Fênix, Itaipulândia, Medianeira, Mirador, Missal, Nova Aliança do Ivaí, Paraíso do Norte, Planaltina do Paraná, Ramilândia, Santa Cruz de Monte Castelo, Santa Isabel do Ivaí, Santa Mônica, São Carlos do Ivaí, Tamboara, Terra Boa and Três Barras do Paraná.

Negative municipalities (60): Altamira do Paraná, Alto Paraná, Amaporã, Anahy, Araruna, Assis Chateaubriand, Boa Esperança, Boa Vista da Aparecida, Braganey, Cafelândia, Campina da Lagoa, Campo Bonito, Campo Largo, Campo Magro, Capitão Leônidas Marques, Catanduvas, Cruzeiro do Sul, Diamante D'Oeste, Diamante do Sul, Engenheiro Beltrão, Entre Rios do Oeste, Espigão Alto do Iguaçu, Formosa do Oeste, Guairaçá, Guaraniaçu, Ibema, Iguatu, Iracema do Oeste, Iretama, Janiópolis, Jesuítas, Lindoeste, Luiziana, Mamborê, Maripá, Matelândia, Mercedes, Nova Aurora, Nova Cantu, Nova Santa Rosa, Palotina, Pato Bragado, Peabiru, Quarto Centenário, Quatro Pontes, Quedas do Iguaçu, Quinta do Sol, Quitandinha, Rancho Alegre D'Oeste, Rio Negro, Roncador, Santa Helena, Santa Lúcia, Santa Tereza do Oeste, São João do Caiuá, São José das Palmeiras, São Pedro do Iguaçu, Serranópolis do Iguaçu, Ubiratã and Vera Cruz do Oeste.

Bahia (Figure 2A)

Biomphalaria glabrata (28): Andaraí, Barra do Choça, Cabaceiras do Paraguaçu, Catu, Entre Rios, Guaratinga, Ibicuí, Iguaí, Itambé, Itapicuru, Itororó, Jiquiriçá, Jitaúna, Lajedo do Tabocal, Maragogipe, Mirangaba, Nova Canaã, Nova Ibiá, Pedrão, Poções, São Desidério, Teodoro Sampaio, Teolândia, Terra Nova, Ubaíra, Utinga, Valença and Vitória da Conquista.

Biomphalaria straminea (14): Aiquara, Barreiras, Barrocas, Casa Nova, Cocos, Coribe, Ipuaú, Itanhém, Jandaira, Juazeiro, Lafaiete Coutinho, Laje, Mutuípe and Vereda.

B. glabrata/B. straminea (32): Anagé, Aporá, Apuarema, Arataca, Baianópolis, Biritinga, Cachoeira, Caem, Cândido Sales, Catolândia, Crisópolis, Esplanada, Feira de Santana, Gandu, Itapetininga, Ituberá, Jacobina, Jequié, Jucuruçu, Lagoa Real, Lamarão, Miguel Calmon, Mundo Novo, Muritiba, Nova Redenção, Potiraguá, Rio Real, Santa Maria da Vitória, São Felix, Serrinha, Wagner and Wenceslau Guimarães.

Negative municipalities (8): Alagoinhas, Araçás, Aramari, Belmonte, Conceição do Jacuípe, Conde, Itanagra and Luiz Eduardo Magalhães.

Pernambuco (Figure 2B)

Biomphalaria straminea (38): Afrânio, Alagoinha, Calumbi, Camocim de São Félix, Capoeiras, Carnaubeira da Penha, Caruaru, Casinhas, Cedro, Cumaru, Dormentes, Feira Nova, Granito, Ibirajuba, Ipubi, Itacuruba, Itaiba, Jaqueira, Jataúba, Jatobá, Joaquim Nabuco, Jucati, Lagoa Grande, Manari, Moreilândia, Orocó, Paranatama, Petrolândia, Poção, Riacho das Almas, Santa Cruz, Santa Filomena, Santa Maria Cambucá, São José da Coroa Grande, São José do Belmonte, Taquaritinga do Norte, Tupanatinga and Xexéu.

B. glabrata/B. straminea (2): Iati and Saire.

Negative municipalities (11): Brejinho, Caetés, Iguaraci, Ingazeira, Quixaba, Santa Cruz da Baixa Verde, Santa Terezinha, São José do Egito, Solidão, Tuparetama and Vertente do Lério.

Rio Grande do Norte (Figure 2C).

Biomphalaria glabrata (1): Baia Formosa.

Biomphalaria straminea (85): Afonso Bezerra, Almino Afonso, Antônio Martins, Areia Branca, Baraúnas, Barcelona, Boa Saúde, Bodó, Bom Jesus, Campo Redondo, Carnaúbas, Coronel Ezequiel, Coronel João Pessoa, Doutor Severiano, Encanto, Equador, Felipe Guerra, Fernando Pedrosa, Francisco Dantas, Frutuoso Gomes, Governador Dix-Sept Rosado, Guamaré, Ipueira, Itajá, Jaçanã, Jandaíra, Januário Cicco, Japi, Jardim de Angicos, João Dias, Judiá, Janduís, Lagoa de Pedras, Lagoa de Velhos, Lagoa Nova, Lagoa Salgada, Lajes, Lajes Pintadas, Lucrécia, Major Sales, Marcelino Vieira, Messias Targino, Montanhas, Monte das Gameleiras, Olho-d'Água dos Borges, Ouro Branco, Paraná, Passa e Fica, Passagem, Pau dos Ferros, Pedra Grande, Pedra Preta, Pilões, Porto do Mangue, Rafael Godeiro, Riacho da Cruz, Riacho de Santana, Riachuelo, Rodolfo Fernandes, Ruy Barbosa, Santana do Seridó, São Bento do Trairi, São Fernando, São Francisco do Oeste, São João do Sabugi, São Pedro, São Rafael, São Vicente, Senador Eloi de Souza, Serra Caiada, Serra de São Bento, Serra do Mel, Serrinha, Serrinha dos Pintos, Severiano Melo, Taboleiro Grande, Tenente Ananias, Tenente Laurentino, Tibau, Timbaúba dos Batistas, Triunfo Potiguar, Umarizal, Upanema, Venha-Ver and Viçosa.

B. glabrata/B. straminea (3): Rio do Fogo, Santa Maria and São Miguel do Gostoso.

Negative municipalities (7): Caiçara do Norte, Carnaúba dos Dantas, Goianinha, Paraú, Patu, Santa Cruz and Tibau do Sul.

Discussion

The results of our study show that the presence of intermediate hosts was recorded in 70.2% of the municipalities studied. The data collected provide additional information - which had been scarce until then - for the archives of the health surveillance teams (http://tabnet.datasus.gov.br/cgi/tabcgi.exe?sinan/pce/cnv/pcebr.def). Notwithstanding, the records provided by this study are in keeping with the known distribution of the three intermediate host species.99. Paraense WL. Planorbídeos hospedeiros intermediários do Schistosoma mansoni. In: Cunha AS, organizadores. Esquistossomose mansoni. São Paulo: Universidade de São Paulo; 1970. It is important to emphasize the simultaneous occurrence of two intermediate S. mansoni host species, namely B straminea and B. glabrata, in 53 municipalities of the five states under analysis. In the case of the state of Rio Grande do Norte, 62% of the information was obtained from the records on the collection of mollusks kept at the Oswaldo Cruz Institute (Fiocruz/CMIOC), reinforcing the importance of the Fiocruz policy of preservation and maintenance of biological collections. On the other hand, mollusks (B. glabrata) infected with S. mansoni were found in only three municipalities out of the 427 studied. Our research confirms: the geographic distribution of these mollusks has been slow, progressively reaching new locations, and corroborates the data obtained by numerous researchers, as well as the data obtained by the National Health Foundation, State Departments of Health and the Ministry of Health Department of Health Surveillance, provided by the managers of the Schistosomiasis Surveillance and Control Program. These databases have been fed by numerous sources and publications.66. Carvalho OS, Scholte RGC, Amaral RS. Distribuição Espacial de Biomphalaria glabrata, B. straminea e B. tenagophila Hospedeiros Intermediários de Schistosoma mansoni no Brasil. In: Carvalho OS, Coelho PMZ, Lenzi HL, (Org.). Schistosoma mansoni e Esquistossomose: uma visão multidisciplinar. 2008. 1 ed. Rio de Janeiro: Fiocruz; 2008; v. 1, p. 529-46.

7. Piza JT, Ramos AS. Os focos autóctones de esquistossomose no Estado de São Paulo. Arq Hig Saúde Pública. 1960; 25:261-71.

8. Schlemper Junior BR, Ferreira Neto JA, Thiago PTS, Bressan C, Amarante AR. Distribuição geográfica de Planorbídeos em Santa Catarina, Brasil. Rev Soc Bras Med Trop. 1996; 29:411-18.

9. Paraense WL. Planorbídeos hospedeiros intermediários do Schistosoma mansoni. In: Cunha AS, organizadores. Esquistossomose mansoni. São Paulo: Universidade de São Paulo; 1970.

10. Paraense WL. Fauna planorbídica do Brasil. In: Lacaz CS, Baruzzi RG, Siqueira Junior W, organizadores. Introdução à geografia médica do Brasil. São Paulo: Edgard Blücher, Universidade de São Paulo; 1972.

11. Paraense WL. The distribution of the molluscan vectors of schistosomiasis in the Americas. Brasília Médica. 1975a;11:11-14.

12. Carvalho OS, Nunes IM, Caldeira RL. First report of Biomphalaria glabrata in the state of Rio Grande do Sul, Brazil. Mem Inst Oswaldo Cruz. 1998; 93:39-40.

13. Paraense WL. The schistosome vectors in the Americas. Mem Inst Oswaldo Cruz. 2001; 96(suppl):7-16.

14. Souza CP, Caldeira RL, Drummond SC, Melo AL, Guimarães CT, Delza MS, Carvalho OS. Geographical Distribution of Biomphalaria Snails in the State of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz. 2001; 96:293-302.

15. Teles HMS, Pereira PAC, Richinitti LMZ. Distribuição de Biomphalaria (Gastropoda, Planorbidade) nos Estados do Rio Grande do Sul e Santa Catarina, Brasil. Rev Saúde Pública de São Paulo. 1991; 25:350-2.

16. Teles HMS. Distribuição geográfica das espécies dos caramujos transmissores de Schistosoma mansoni no Estado de São Paulo, Brasil. Rev Soc Bras de Med Trop. 2005; 38:426-32.

17. Thiengo SC, Fernandez MA, Boaventura MFF, Stortti MA. A survey of freshwater gastropods in the Serrana Mesoregion of the state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 1998; 93(supl I):233-4.

18. Thiengo SC, Fernandez MA, Boaventura MFF, Grault CE, Silva HF, Mattos AC, Santos SB. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: I - Metropolitan mesoregion. Mem Inst Oswaldo Cruz. 2001;96:177-84.

19. Thiengo SC, Fernandez MA, Boaventura MFF, Magalhães MG, Santos SB. Freshwater snails and Schistosomiasis mansoni in the state of Rio de Janeiro, Brazil: III - Baixadas Mesoregion. Mem Inst Oswaldo Cruz. 2002a; 97:43-6.

20. Thiengo SC, Fernandez MA, Boaventura MFF, Silva HF, Mattos AC, Santos SB. Freshwater snails and Schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: II - Centro Fluminense Mesoregion. Mem Inst Oswaldo Cruz. 2002b(5);97:621-6.

21. 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. 2004; 99:275-80.

22. 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(supl. I):239-45.

23. 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; 22:867-74.
-2424. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Vigilância e controle de moluscos de importância epidemiológica. Diretrizes técnicas: programa de Vigilância e Controle da Esquistossomose (PCE). Brasília: Ministério da Saúde; 2008.

In spite of the efforts made, data about the actual geographic distribution of these mollusks throughout all the national territory are subject both to the difficulty of access to certain regions of the country and the lack of financial resources and limited number of researchers working in this specific area. Another major limitation lies in the capacity of intermediate hosts of S. mansoni to adapt to inappropriate environmental conditions, such as drought in their habitats, thus imposing the need of conducting periodic searches in freshwater biotopes.2828. Paraense WL. Self and cross-fertilization in Australorbis glabratus. Mem Inst Oswaldo Cruz. 1955;53:285-91. These mollusks are able to bury themselves as the environment becomes drier; while after the rainy season, they quickly repopulate the habitat thanks to their great reproductive capacity. According to Paraense,2828. Paraense WL. Self and cross-fertilization in Australorbis glabratus. Mem Inst Oswaldo Cruz. 1955;53:285-91. a single B. glabrata specimen is capable of cumulatively producing ten million descendants in three months. Besides burying themselves, these mollusks can survive even if they are infected with S. mansoni, by reducing their metabolism and remaining in diapause or anhydrobiosis.2929. Barbosa FS, Coelho MV. Ação de dessecação sobre as fases larvárias intracaramujo de Schistosoma mansoni em Australorbis glabratus. Pub Av Inst Aggeu Magalhães. 1953; 11:159-62. The geographical distribution of S. mansoni intermediate hosts in Brazil provides schistosomiasis with the ability to spread, including to areas considered to be unaffected.66. Carvalho OS, Scholte RGC, Amaral RS. Distribuição Espacial de Biomphalaria glabrata, B. straminea e B. tenagophila Hospedeiros Intermediários de Schistosoma mansoni no Brasil. In: Carvalho OS, Coelho PMZ, Lenzi HL, (Org.). Schistosoma mansoni e Esquistossomose: uma visão multidisciplinar. 2008. 1 ed. Rio de Janeiro: Fiocruz; 2008; v. 1, p. 529-46.,99. Paraense WL. Planorbídeos hospedeiros intermediários do Schistosoma mansoni. In: Cunha AS, organizadores. Esquistossomose mansoni. São Paulo: Universidade de São Paulo; 1970.,3030. Carvalho OS, Rocha RS, Massara CL, Katz N. Primeiros casos autóctones de esquistossomose mansoni em região do Noroeste do Estado de Minas Gerais. Rev Saúde Pública São Paulo. 1988; 22:237-9.

The geographical distribution and the correct identification of three intermediate S. mansoni host species are important to guide health care workers and the surveillance and environmental control measures in each locality, allowing the interruption of the disease’s epidemiological chain. Studies like this one contribute to health services in terms of improving or more appropriate structuring of schistosomiasis control and surveillance activities, directing actions toward areas of risk and streamlining the application of resources available. S. mansoni intermediate host mollusk monitoring activities and research into of larval forms of S. mansoni need to be permanent activities, as preventive measures to prevention the spread or outbreaks of schistosomiasis in Brazil.

Acknowledgments

State Health Departments of Paraná, Minas Gerais, Bahia, Pernambuco and Rio Grande do Norte, for the logistical support to the accomplishment of this work.

José Geraldo Amorim da Silva, of the René Rachou Institute/Oswaldo Cruz Foundation/Helminthology and Medical Malacology Labortory, for his technical support.

References

  • 1
    Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Vigilância da Esquistossomose Mansoni: Diretrizes Técnicas. 4. ed. Brasília: Ministério da Saúde, 2014.
  • 2
    Paraense WL. Distribuição dos caramujos no Brasil. In: Reis FA, Faria I, Katz N, organizadores. Modernos Conhecimentos sobre Esquistossomose Mansônica. Belo Horizonte: Academia Mineira de Medicina; 1986; v. 1, p.117-128.
  • 3
    Corrêa LR, Paraense WL. Susceptibility of Biomphalaria amazonica to infection with two strains of Schistosoma mansoni Rev Inst Med Trop São Paulo. 1971;13:387-90.
  • 4
    Paraense WL, Corrêa LR. Susceptibility of Biomphalaria peregrina from Brazil and Ecuador to two strains of Schistosoma mansoni Rev Inst Med Trop São Paulo. 1973; 15:127-30.
  • 5
    Teodoro TM, Jannotti-Passos LK, Carvalho OS, Caldeira RL. Occurrence of Biomphalaria cousini (Mollusca: Gastropoda) in Brazil and its susceptibility to Schistosoma mansoni (Platyhelminths: Trematoda). Mol Phyl Evol. 2010; 57:144-51.
  • 6
    Carvalho OS, Scholte RGC, Amaral RS. Distribuição Espacial de Biomphalaria glabrata, B. straminea e B. tenagophila Hospedeiros Intermediários de Schistosoma mansoni no Brasil. In: Carvalho OS, Coelho PMZ, Lenzi HL, (Org.). Schistosoma mansoni e Esquistossomose: uma visão multidisciplinar. 2008. 1 ed. Rio de Janeiro: Fiocruz; 2008; v. 1, p. 529-46.
  • 7
    Piza JT, Ramos AS. Os focos autóctones de esquistossomose no Estado de São Paulo. Arq Hig Saúde Pública. 1960; 25:261-71.
  • 8
    Schlemper Junior BR, Ferreira Neto JA, Thiago PTS, Bressan C, Amarante AR. Distribuição geográfica de Planorbídeos em Santa Catarina, Brasil. Rev Soc Bras Med Trop. 1996; 29:411-18.
  • 9
    Paraense WL. Planorbídeos hospedeiros intermediários do Schistosoma mansoni In: Cunha AS, organizadores. Esquistossomose mansoni. São Paulo: Universidade de São Paulo; 1970.
  • 10
    Paraense WL. Fauna planorbídica do Brasil. In: Lacaz CS, Baruzzi RG, Siqueira Junior W, organizadores. Introdução à geografia médica do Brasil. São Paulo: Edgard Blücher, Universidade de São Paulo; 1972.
  • 11
    Paraense WL. The distribution of the molluscan vectors of schistosomiasis in the Americas. Brasília Médica. 1975a;11:11-14.
  • 12
    Carvalho OS, Nunes IM, Caldeira RL. First report of Biomphalaria glabrata in the state of Rio Grande do Sul, Brazil. Mem Inst Oswaldo Cruz. 1998; 93:39-40.
  • 13
    Paraense WL. The schistosome vectors in the Americas. Mem Inst Oswaldo Cruz. 2001; 96(suppl):7-16.
  • 14
    Souza CP, Caldeira RL, Drummond SC, Melo AL, Guimarães CT, Delza MS, Carvalho OS. Geographical Distribution of Biomphalaria Snails in the State of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz. 2001; 96:293-302.
  • 15
    Teles HMS, Pereira PAC, Richinitti LMZ. Distribuição de Biomphalaria (Gastropoda, Planorbidade) nos Estados do Rio Grande do Sul e Santa Catarina, Brasil. Rev Saúde Pública de São Paulo. 1991; 25:350-2.
  • 16
    Teles HMS. Distribuição geográfica das espécies dos caramujos transmissores de Schistosoma mansoni no Estado de São Paulo, Brasil. Rev Soc Bras de Med Trop. 2005; 38:426-32.
  • 17
    Thiengo SC, Fernandez MA, Boaventura MFF, Stortti MA. A survey of freshwater gastropods in the Serrana Mesoregion of the state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 1998; 93(supl I):233-4.
  • 18
    Thiengo SC, Fernandez MA, Boaventura MFF, Grault CE, Silva HF, Mattos AC, Santos SB. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: I - Metropolitan mesoregion. Mem Inst Oswaldo Cruz. 2001;96:177-84.
  • 19
    Thiengo SC, Fernandez MA, Boaventura MFF, Magalhães MG, Santos SB. Freshwater snails and Schistosomiasis mansoni in the state of Rio de Janeiro, Brazil: III - Baixadas Mesoregion. Mem Inst Oswaldo Cruz. 2002a; 97:43-6.
  • 20
    Thiengo SC, Fernandez MA, Boaventura MFF, Silva HF, Mattos AC, Santos SB. Freshwater snails and Schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: II - Centro Fluminense Mesoregion. Mem Inst Oswaldo Cruz. 2002b(5);97:621-6.
  • 21
    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. 2004; 99:275-80.
  • 22
    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(supl. I):239-45.
  • 23
    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; 22:867-74.
  • 24
    Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Vigilância e controle de moluscos de importância epidemiológica. Diretrizes técnicas: programa de Vigilância e Controle da Esquistossomose (PCE). Brasília: Ministério da Saúde; 2008.
  • 25
    Deslandes N. Técnica de dissecação e exame de planorbídeos. Rev Serv Espec Saúde Pública. 1950;4:371-82.
  • 26
    Paraense WL. Estado atual da sistemática dos planorbídeos brasileiros. Arq Mus Nac. 1975b;55:105-28.
  • 27
    Vidigal T, Caldeira RL, Simpson AJG, Carvalho OS. Further studies on the molecular systematic of Biomphalaria snails from Brazil. Mem Inst Oswaldo Cruz. 2000;95:57-66.
  • 28
    Paraense WL. Self and cross-fertilization in Australorbis glabratus Mem Inst Oswaldo Cruz. 1955;53:285-91.
  • 29
    Barbosa FS, Coelho MV. Ação de dessecação sobre as fases larvárias intracaramujo de Schistosoma mansoni em Australorbis glabratus Pub Av Inst Aggeu Magalhães. 1953; 11:159-62.
  • 30
    Carvalho OS, Rocha RS, Massara CL, Katz N. Primeiros casos autóctones de esquistossomose mansoni em região do Noroeste do Estado de Minas Gerais. Rev Saúde Pública São Paulo. 1988; 22:237-9.

  • *
    This project was funded by the Department of Health Surveillance of the Brazilian Ministry of Health (National Health Foundation/Ministry of Health: Term of Cooperation No. 173/2010), René Rachou Institute/Oswaldo Cruz Foundation/Belo Horizonte, MG, and Oswaldo Cruz Institute/Oswaldo Cruz Foundation/Rio de Janeiro, RJ. The project was carried out in accordance with article 14 of Law No. 5,197, dated 3 January 1967 ('Law of Fauna'), which provides for the granting to scientists belonging to scientific institutions, a special license for collecting material for scientific purposes.

Publication Dates

  • Publication in this collection
    22 Oct 2018

History

  • Received
    04 Oct 2017
  • Accepted
    25 May 2018
Secretaria de Vigilância em Saúde - Ministério da Saúde do Brasil Brasília - Distrito Federal - Brazil
E-mail: leilapgarcia@gmail.com