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Revista do Instituto de Medicina Tropical de São Paulo

On-line version ISSN 1678-9946

Rev. Inst. Med. trop. S. Paulo vol.55 no.6 São Paulo Nov./Dec. 2013

http://dx.doi.org/10.1590/S0036-46652013000600006 

PHLEBOTOMINES

PHLEBOTOMINE SANDFLIES IN RURAL LOCATIONS IN THE STATE OF PARANA, SOUTHERN BRAZIL

Flebotomíneos em localidades rurais do Estado do Paraná, Sul do Brasil

Simone Cristina Castanho Sabaini de Melo1 

Wilsandrei Cella2 

Rubens Massafera3 

Natália Maria Maciel Guerra Silva1 

Reinaldo Marqui4 

Maria Dalva de Barros Carvalho5 

Ueslei Teodoro5 

1Universidade Estadual do Norte do Paraná Campus Luiz Meneghel, simonecastanho@uenp.edu.br, natyguerra@uenp.edu.br, Universidade Estadual do Norte do Paraná, Luiz Meneghel. E-mails:, simonecastanho@uenp.edu.br, natyguerra@uenp.edu.br

2Universidade Paranaense Campus Cianorte, wilsandrei_bio@hotmail.com, Universidade Paranaense, Cianorte. E-mail:, wilsandrei_bio@hotmail.com

3Núcleo de Entomologia de Jacarezinho. Secretaria de Estado da Saúde do Paraná. E-mail:rubensmassafera-@hotmail.comrubensmassafera-@hotmail.com

4Secretaria Municipal de Saúde de Bandeirantes. E-mail:reimarquibio@hotmail.comreimarquibio@hotmail.com

5Universidade Estadual de Maringá. E-mails:mdbcarvalho@uem.bruteodoro@uem.brmdbcarvalho@uem.bruteodoro@uem.br


ABSTRACT

SUMMARY

This study reports the fauna and frequency of sandflies in domestic animal shelters, residences and other ecotopes in rural areas of the municipality of Bandeirantes, Paraná State. Sandflies were collected twice in eight rural villages by using Falcon traps from 8pm to 6am in 2008. In these localities 4,790 sandflies were collected, which were represented by ten sandfly species, prevailing of Nyssomyia neivai and Nyssomyia whitmani species. It was observed that animal shelters are the domestic ecotopes where there is the greatest frequency of these insects. The localities where the collections were made had the environmental characteristics that allow the persistence of transmission of parasites from the American tegumentary leishmaniasis. Although the fauna and the behavior of sandflies species are similar in different localities, the method of controlling these insects should be adjusted to the environmental characteristics of each one of the most diverse endemic areas of American tegumentary leishmaniasis in the municipalities of Paraná State.

Key words: Sandflies; American Tegumentary Leishmaniasis; Leishmania ; Animal's shelter; Fauna; Control

RESUMO

RESUMO

Relatam-se, neste trabalho, a fauna e frequência de flebotomíneos em abrigos de animais domésticos, residências e outros ecótopos em áreas rurais do município de Bandeirantes, Estado do Paraná. Os flebotomíneos foram coletados em oito bairros rurais, com armadilhas de Falcão, duas vezes em cada bairro, das 20 às 6 horas, em 2008. No conjunto dos bairros coletaram-se 4.790 flebotomíneos, representados por dez espécies, com predomínio de Nyssomyia neivai e Nyssomyia whitmani. Os abrigos dos animais domésticos são os ecótopos onde há maior frequência desses insetos. As localidades onde as coletas foram realizadas têm características ambientais que permitem a persistência da transmissão de parasitos da leishmaniose tegumentar americana. Apesar da fauna e do comportamento das espécies de flebotomíneos serem semelhantes nas diversas localidades, o método de controle desses insetos deve ser ajustado às características ambientais de cada uma das mais diversas áreas endêmicas de leishmaniose tegumentar americana, nos municípios do Paraná.

INTRODUCTION

The leishmaniasis condition is sited among the top five diseases that have a major impact on public health worldwide14. In Latin America, the cutaneous leishmaniasis (CL) has a strong impact on public health, especially in Brazil, where it occurs in every State12. In the State of Paraná, CL is an endemic disease and it has been registered in more than 300 of the 399 municipalities10 including the municipality of Bandeirantes.

In Bandeirantes municipality, 232 autochthonous cases of TL were noted, with yearly occurrences from 1990 to 2009. As a result, this research on phlebotomine fauna and frequency in domiciliary, peridomiciliary and rural localities was conducted in order to provide detailed knowledge on the areas where the leishmania transmissions have happened that could be helpful when choosing the most effective method to control the vectors.

MATERIAL AND METHODS

Municipality description: The municipality of Bandeirantes is located in the North Pioneer mesoregion of Paraná and according to the Demographic Census conducted in 2010, has a population of 32,182 inhabitants, of which 28,382 are living in urban and 3,800 in rural areas. The vegetation type of the municipality is of semi-deciduous forest and the soil is a composite type (Red Podzol, Red Latosol and Red Nitosol). The climate is subtropical humid reaching in the coldest month averaged temperatures lower than 18 °C and in the warmest month averaging higher than 22 °C. The municipality has an area of 44,527.9 hectares (ha), where only 872.9 ha are native forest. Nowadays, 80% of the municipality's territory is occupied by grain crops (soya and maize), alfalfa and sugar cane. According to Figure 1, the rural zone of Bandeirantes is divided into 17 districts, of which eight of them (Água da Jacutinga, Água das Perobas, São Paulo, Cabiúna, Água do Cateto, Água do Caixão, Água Vermelha and Água da Boa Pastora) were selected for collection of sandflies. In these districts in Água do Caixão and Água da Boa Pastora there were no reported cases of CL.

Fig. 1 Água da Jacutinga, Água das Perobas, São Paulo, Cabiúna, Água do Cateto, Água Vermelha, Água do Caixão and Água da Boa Pastora localities, where Phlebotomine sandflies were collected in the city of Bandeirantes, State of Paraná, Brazil. 

Rural neighborhoods where the phlebotomines were collected:

  1. Água da Jacutinga (23° 05′S/50° 25′W). Two farms were selected from which to collect the samples: (3 irmãos Farm and Silva Farm). In the first one, the traps were installed in the woods 984.25m from a house (E1); in a chicken coop (E2); 9.84m from a house (E3), and in a pigsty 6.56m from this same house (E4). In the second farm, the traps were installed in a pigsty 64.04m from a house (E5); in the woods, 984.25m from the same house (E6); in a house made of wood which is used as chicken coop and is 6.56m from another house (E7), and in a banana plantation (E8). In both farms there are soybean and sugar cane plantations.

  2. Água das Perobas (23° 14′S/50° 18′W). Samples were collected in Peroba Farm. The traps were installed in sites (E1, E2 and E4) which were located behind the houses (E3, E5, E6, E9) where traps were also installed; in chicken coops (E7, E8) 6.56m from these houses, and in the woods, 984.25m from the same houses.

  3. São Paulo (23° 10′S/50° 16′W). Samples were collected in three farms: Santo Antônio, Boa Esperança and Santa Rita. In the first one, the traps were installed in a house (E1) and in a pigsty (E2) 164.04m from a house. In the second farm, the collection was taken in a chicken coop (E3) 6.56m from a house; in a pigsty (E4) 16.4m from a house; in a chicken coop (E5) 9.84m from the same house, and in a corral (E6) 16.4m from another house. In Santa Rita Farm, the samples were collected in a chicken coop (E7) 9.84m from a house; 3.8m from a pigsty (E8); in a house (E9), and in a chicken coop (E10) 6.56m from a house.

  4. Cabiúna. (23° 13′S/50° 23′W). The phlebotomine collection was taken in Durval Mariquito Farm, Lazarini Farm and in Santa Maria Farm. In the first one, the collection was taken in a pigsty (E1) 16.4m from a house (E4 and E5), where traps were also installed. In the woods (E2) 164.04m from these houses; in a chicken coop (E3) 9.84m from those houses. In Lazarini Farm, the samples were collected in a house (E6) and in a chicken coop (E7) 6.56m from E6 and 1,148.29 m from the woods. In Santa Maria farm, the collection was taken in a house (E8), in a pigsty (E9) 6.56m from a house and 984.25m from the woods and in a chicken coop (E10).

  5. Água do Cateto (23° 12′S/50° 18′W). The collection was taken in Cateto Nomura Farm in houses (E1, E2, E5, E8 and E9); in chicken coops close to these houses (E3, E4 and E7); in a pigsty (E6) near these same houses, and in a corral (E10). Considering all the localities where the work was done, this one has the largest residual area, which is located approximately 656.17m from the residences.

  6. Água Vermelha (23° 09′S/50° 26′W). The collect was done in Boa Vista Farm in houses (E1, E2, E6 and E8); chicken coops (E3 and E9); in pigsty (E4) 196.85m from the woods (E5), in a hangar (E7), and in a dam shore (E10) 6.56m from the woods.

  7. Água do Caixão (23° 06′S/50° 20′W). The collections were done in Tanaka Farm, in two houses (E1, E6); in a chicken Coop (E2); in a corral linked to a pigsty (E3); in a duck barn (E4); in canebrakes (E5, E8); in a pigsty (E7) and in hangars (E9, E10). The house (E1) was 6.56m from the chicken coop (E2) and the corral linked to the pigsty (E3). The pigsty was located 6.56m from E6.

  8. Água da Boa Pastora (23° 08′S/50° 22′W). The phlebotomines collection was done in São Luiz Farm, Francisco Marques and Bela Manhã Farms. In the first one, in a chicken coop (E1) and in a house (E2). In Francisco Marques Farm, the collection was done in a goat barn (E3); in a pigsty (E4); in a house (E5) and in a chicken coop (E6). In the last one, in a pigsty (E7); in a chicken coop (E8) and in two houses (E9, E10).

Collection and phlebotomines identification: The phlebotomines were caught in 15 localities distributed between eight rural neighborhoods. During area selection, in order to implement the capture, six disease registers in humans were found in two of these areas and in two of them there was no occurrence. The collection was done with a light trap, from 8pm to 6am, from January to March and September to December of 2008, and it consisted of two collections per locality (20 hours).

The number of traps installed in each locality varied from eight to ten because of each house's availability and other ecotopes in the peridomiciliary area. The collected specimens were sacrificed in chloroform and then kept in cardboard boxes containing mothballs. Phlebotomines were prepared and identified in the Medical Entomology Laboratory of 19th Health Dept. of Jacarezinho, Parana State. The nomenclature follows GALATI3and abbreviation follows MARCONDES6.

RESULTS

A total of 4,790 phlebotomines, belonging to 11 species, were collected: Nyssomyia neivai, Nyssomyia whitmani, Pintomyia pessoai, Migonemyia migonei, Pintomyia fischeri, Evandromyia cortelezzii, Micropygomyia ferreirana, Expapillata firmatoi, Brumptomyia brumpti, Evandromyia sallesi and Brumptomyia cunhai. The hourly average (HA) of total phlebotomines collected was 239.5 (Table 1).

Tabela 1 Phlebotomine sandflies species collected in rural localities in the city of Bandeirantes, State of Paraná, from January to December of 2008 

Specie/Zone/Hourly Average AJ HA AP HA SP HA CA HA AC HA AV HA AX HA AB HA Total HA
Nyssomyia neivai 104 5.20 99 4.95 112 5.60 10 0.50 1,144 57.20 192 9.60 48 2.40 385 19.25 2,093 104.70
Nyssomyia whitmani 31 1.55 135 6.75 113 5.65 21 1.05 968 48.40 210 10.50 21 1.05 440 22.00 1,939 96.95
Pintomyia pessoai 21 1.05 388 19.40 6 0.30 - - 51 2.55 16 0.80 - - 43 2.15 525 26.25
Migonemyia migonei 7 0.35 23 1.15 11 0.55 3 0.15 53 2.65 4 0.20 1 0.05 10 0.50 112 5.60
Pintomyia fischeri 6 0.30 27 1.35 2 0.10 - - 35 1.75 6 0.30 - - 1 0.05 71 3.55
Evandromyia cortelezzii 4 0.20 4 0.20 - - - - - - - - - - - - 8 0.40
Micropygomyia ferreirana 12 0.60 2 0.10 1 0.05 - - - - - - - - - - 15 0.75
Expapillata firmatoi 8 0.40 - - - - - - - - 3 0.15 - - - - 11 0.55
Brumptomyia cunhai - - 7 0.35 - - - - - - - - - - - - 7 0.35
Brumptomyia brumpti 1 0.05 - - - - - - - - - - - - - - 1 0.05
Evandromyia sallesi 1 0.05 - - - - - - - - - - - - - - 1 0.05
Total 195 9.75 685 34.25 245 12.25 34 1.70 2,251 112.55 431 21.55 70 3.50 879 43.95 4,790 239.50

AJ = Água da Jacutinga; AP = Água das Perobas; SP = São Paulo; CA = Cabiúna; AC = Água do Cateto; AV = Água Vermelha; AX = Água do Caixão; AB = Água da Boa Pastora; HA = Hourly Average.

In the Água do Cateto, Água da Boa Pastora and Água das Perobas neighborhoods 79.6% (HA = 190.20) of its total was collected. The most frequent species collected were Ny. neivai (HA = 104.70), Ny. whitmani (HA = 96.95) and Pi. pessoai (HA = 26.25) (Table 1).

In its total neighborhood set 1,788 (HA = 89.40) phlebotomines were collected in 20 chicken coops, 1,350 (HA = 67.50) in 15 piggeries and 973 (HA = 48.65) in 26 house porches (Table 2).

Tabela 2 Phlebotomine sandflies collected in several environments, in rural localities in the city of Bandeirantes, State of Paraná, from January to December of 2008 

Environments/sites AJ HA AP HA SP HA CA HA AC HA AV HA AX HA AB HA Total HA
Hennery 49 2.45 11 0.55 76 3.80 1 0.05 1,563 78.15 14 0.70 2 0.10 85 4.25 1,788 89.40
Piggery 103 5.15 152 7.60 46 2.30 - - 292 14.60 235 11.75 31 1.55 491 24.55 1,350 67.50
Houses 15 0.75 139 6.95 3 0.15 13 0.65 391 19.55 169 8.45 - - 243 12.15 973 48.65
Woods 28 1.40 383 19.15 - - 20 1.00 - - 4 0.20 - - - - 435 21.75
Corrals - - - - 120 6.00 - - - - - - - - - - 120 6.00
Goat shelter - - - - - - - - - - - - - - 60 3.00 60 3.00
Corral/Piggery - - - - - - - - - - - - 29 1.45 - - 29 1.45
Banana tree - - - - - - - - - - - - - - - - 13 0.65
Mango tree - - - - - - - - 5 0.25 - - - - - - 5 0.25
Water reservoir margin - - - - - - - - - - 5 0.25 - - - - 5 0.25
Sheds - - - - - - - - - - 4 0.20 2 0.10 - - 6 0.30
Bamboo plantation - - - - - - - - - - - - 4 0.20 - - 4 0.20
Duck shelter - - - - - - - - - - - - 2 0.10 - - 2 0.10
Total 195 9.75 685 34.25 245 12.25 34 1.70 2,251 112.55 431 21.55 70 3.50 879 43.95 4,790 239.50

AJ = Água da Jacutinga; AP = Água das Perobas; SP = São Paulo; CA = Cabiúna; AC = Água do Cateto; AV = Água Vermelha; AX = Água do Caixão; AB = Água da Boa Pastora; HA = Hourly Average.

DISCUSSION

The eleven species collected in several districts of the municipality of Bandeirantes has already been described in several municipalities of Paraná State7 11-12, including in Peroba Farm (Água das Perobas locality)8.

The Ny. neivai, Ny. whitmani, Mi. migonei, Pi. pessoai and Pi. fischeri phlebotomines have a very common occurrence in many endemic areas of CL in Paraná State1 11-12, demonstrating that these species of phlebotomine sand flies present genetic characteristics that allow them to adapt to anthropogenic environments with distinct levels of changes and due to “a sort of” spatial, olfactory memory and/or to the host fidelity that direct them to recognize environments of blood supply, rest and reproduction2. The first four species were already marked with natural infection by protozoa of Leishmania genus in other regions of Brazil, showing the potential of vector insects in natural and anthropogenic environments4 6. The natural infection of Ny. whitmani was observed in Paraná State4 and Ny. neivai in Paraná and Santa Catarina States5 9.

In the majority of the districts where the phlebotomine collections were made in bad hygiene condition homes the presence of humidity and organic matter in the soil (leaves, fruits, domestic animal feces, food and vegetal waste) of domestic animals shelters and residences in the neighborhoods of remaining forests was noticed in the peridomicile. These factors are crucial for the formation of phlebotomine breeding sites that invade domiciles6 10 13, increasing the vulnerability of the inhabitants to the CL.

CONCLUSION

In the neighborhoods where the collections were done, 10 phlebotomines species were found, and, among those, Ny. neivai and Ny. whitmani were the main ones. Domestic animal shelters are the ecotopes where these insects frequency occurs the most. The localities where the collections were done have environmental characteristics that allow Leishmania transmission persistence.

Even though fauna and phlebotomines species behavior are similar in many localities, the control method of these insects has to be adjusted to the environmental characteristics of each CL endemic area in Paraná municipalities.

The detailed knowledge on the localities where there is leishmaniasis transmission chain gives the public health administration the option to choose more efficient methods in order to control the spread of the disease. The municipalities have not maintained their promise when it comes to the endemic control of diseases that involve vectors, and it shows the demand for changes in Ministry of Health policies. The increase of cases of diseases related to these insects shows the need to capacitate community health agents for vector vigilance development activities.

Acknowledgements

To the Healthcare agents of the Entomology Group of the municipality of Jacarezinho/Secretary of Health of the State of Paraná, Mr. Hélio Aparecido Barbosa, Nivaldo Paulino, and Valdeci Aparecido Fagundes for their assistance in collection and identification of sandflies and to the Technical in Health Surveillance, Mr. Edson Carlos Capi in supporting the orientation process of the localities where the collections were made.

REFERENCES

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2. Freitas JS, Reinhold-Castro KR, Casanova C, Silva JP, Previdelli I, Teodoro U. Memória espacial e/ou olfativa em flebotomíneos em área endêmica de leishmaniose tegumentar americana, sul do Brasil. Rev Soc Bras Med Trop. 2009;42:151-5. [ Links ]

3. Galati EAB. Morfologia e taxonomia. In: Rangel EF, Lainson R, editores. Flebotomíneos do Brasil. Rio de Janeiro: Editora Fiocruz; 2003. p. 23-51. [ Links ]

4. Luz E, Membrive N, Castro EA, Dereure J, Pratlong F, Dedet JA, et al. Lutzomyia whitmani (Diptera: Psychodidae) as vector of Leishmania (V). braziliensis in Paraná State, Southern Brazil. Ann Trop Med Parasitol. 2000;94:623-31. [ Links ]

5. Marcondes CB, Bittencourt IA, Stoco PH, Eger I, Grisard EC, Steindel M. Natural infection of Nyssomyia neivai (Pinto, 1926) (Diptera: Psychodidae, Phlebotominae) by Leishmania (Viannia) spp. in Brazil. Trans R Soc Trop Med Hyg. 2009;103:1093-7. [ Links ]

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7. Massafera R, Silva AM, Carvalho AP, Santos DR, Galati EAB, Teodoro U. Fauna de flebotomíneos do município de Bandeirantes, no Estado do Paraná. Rev Saúde Pública. 2005;39:571-7. [ Links ]

8. Membrive NA, Rodrigues G, Membrive U, Monteiro WM, Neitzke HC, Lonardoni MVC, et al. Flebotomíneos de municípios do norte do Estado do Paraná, sul do Brasil. Entomol Vec. 2004;11:673-80. [ Links ]

9. Oliveira DM. Padronização de técnicas moleculares para o diagnóstico e epidemiologia de leishmaniose tegumentar americana. [dissertação]. Maringá: Universidade Estadual de Maringá; 2009. [ Links ]

10. Reinhold-Castro KR, Scodro RB, Dias-Sversutti AC, Neitzke HC, Rossi RM, Kühl JB, et al. Avaliação de medidas de controle de flebotomíneos. Rev Soc Bras Med Trop. 2008;41:269-76. [ Links ]

11. Silva AM, Camargo NJ, Santos DR, Massafera R, Ferreira AC, Posta C, et al. Diversidade, distribuição e abundância de flebotomíneos (Diptera: Psychodidae) no Paraná. Neotrop Entomol. 2008;37:209-25. [ Links ]

12. Teodoro U, Santos DR, Santos AR, Oliveira O, Poiani LP, Silva AM, et al. Informações preliminares sobre flebotomíneos do norte do Paraná. Rev Saúde Pública. 2006;40:327-30. [ Links ]

13. Teodoro U, Santos DR, Santos AR, Oliveira O, Santos ES, Neitzke HC, et al. Avaliação de medidas de controle de flebotomíneos no Município de Lobato, Estado do Paraná, Sul do Brasil. Cad Saúde Pública. 2006;22:451-5. [ Links ]

14. World Health Organization. Leishmaniasis: magnitude of the problem. [cited 2008 Nov 08]. Available from: http://www.who.int/leishmaniasis/burden/magnitude [ Links ]

Financial support given by CNPq (Proc. 410550/2006-0).

Received: August 15, 2012; Accepted: April 15, 2013

Correspondence to: Simone C. Castanho S. de Melo, R. São Paulo 801, Vila Paraíso, 86360-000 Bandeirantes, PR, Brasil. E-mail: simonecastanho@uenp.edu.br

Creative Commons License This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.