Sandfly frequency in a clean and well-organized rural environment in the state of Paraná, Brazil

Frequência de flebotomíneos em ambiente rural com boas condições de limpeza e organização, no estado do Paraná, Brasil

ARTICLE ARTIGO

Sandfly frequency in a clean and well-organized rural environment in the state of Paraná, Brazil

Frequência de flebotomíneos em ambiente rural com boas condições de limpeza e organização, no estado do Paraná, Brasil

Cristiane Machado de Oliveira Legriffon^I; Kárin Rosi Reinhold-Castro^I; Vanderson Carvalho Fenelon^II; Herintha Coeto Neitzke-Abreu^I; Ueslei Teodoro^I

^IPrograma de Pós-Graduação em Ciências da Saúde, Universidade Estadual de Maringá, Maringá, PR

^IICurso de Farmácia, Universidade Estadual de Maringá, Maringá, PR

^{Address to}

ABSTRACT

INTRODUCTION: Sandflies caught in Santa Juliana Farm in Sarandi, State of Paraná, Brazil, were assessed in terms of their fauna, seasonality, and frequency in the homes and in shelters of domestic animals around the homes, as well as in the nearby forest.

METHODS: In Santa Juliana Farm, there are no records of cases of ACL, differing from other relatively clean and organized areas where surveys of sandflies have been conducted in Paraná. Samples were collected with Falcão light traps, fortnightly from 22:00 to 02:00 hours, from November 2007 to November 2008.

RESULTS: A total of 4,506 sandflies were captured, representing 13 species, predominantly Nyssomyia whitmani (71.8%). More sandflies were collected in the forest (52.6%) than outside the forest (residences and pigsty) (47.4%). However, Ny. whitmani was collected in greater numbers outside (38.3%) than inside the forest (33.5%). Most sandflies were collected in the warmer months and during periods with regular rainfall.

CONCLUSIONS: The results suggest that cleaning and organization around the houses could reduce sandfly population in peridomicile. Constructing shelters for animal at a distance of approximately 100m from domiciles is recommended to prevent the invasion of sandflies, as this farm has an area of preserved forest, with wild animals and sandflies present to maintain the enzootic cycle of Leishmania.

Keywords: Phlebotominae. Vectors ecology. Control of leishmaniasis.

RESUMO

INTRODUÇÃO: Relatam-se os resultados de coletas de flebotomíneos na Fazenda Santa Juliana, município de Sarandi, Estado do Paraná, Brasil, onde se verificou a fauna, a sazonalidade e a frequência desses insetos nos ambientes florestal e extraflorestal.

MÉTODOS: O trabalho foi realizado nesta fazenda pela inexistência de registro de casos de LTA e por diferir de outras áreas onde foram realizadas pesquisas com flebotomíneos, no Paraná, e pela limpeza e organização do peridomicílio. As coletas foram realizadas com sete armadilhas luminosas de Falcão, quinzenalmente das 22 às 2 horas, de novembro de 2007 a novembro de 2008.

RESULTADOS: Foram capturados 4.506 flebotomíneos de 13 espécies, com predomínio de Nyssomyia whitmani (71,8%). Coletou-se maior proporção de flebotomíneos no ambiente florestal (52,6%) do que no extraflorestal (residências e chiqueiro) (47,4%), entretanto a proporção de Ny. whitmani coletada foi maior no ambiente extraflorestal (38,3%) do que no florestal (33,5%). A maioria dos flebotomíneos foi coletada nos meses mais quentes e com quedas regulares de chuva.

CONCLUSÕES: Os resultados sugerem que a limpeza e a organização do peridomicílio podem auxiliar a reduzir a população de flebotomíneos no domicílio e no peridomicílio, recomendando-se que a construção de abrigos de animais guarde a distância aproximada de 100m das residências, para evitar a invasão desses insetos, uma vez que nesta fazenda existe uma área de mata de preservação, com a presença de animais silvestres e flebotomíneos, que mantem o ciclo enzoótico de Leishmania.

Palavras-chaves: Flebotomíneos. Ecologia de vetores. Controle de leishmanioses.

INTRODUCTION

Leishmaniases are among the six tropical diseases of major public-health significance. They are caused by protozoans of the genus Leishmania, which exploit wild mammals (reservoirs) and sandflies (vectors) in their natural life cycles^1,2. In Latin America, where the number of cases of American cutaneous leishmaniasis (ACL) has remained relatively high, Brazil accounts for most cases, with 527,976 persons affected from 1990 to 2008³. Of these, 12,115 were recorded in Southern Brazil - 95.4% of them in the State of Paraná³.

The large number and wide distribution of ACL cases in Brazil underscore the importance of studies on the control of sandflies. Traditionally, sandfly control has been accomplished with the use of chemical insecticides^4-7. However, these measures have been proven ineffective for use during interrupted and/or inappropriate periods^8-10.

In Paraná^11-14 and in other states of Brazil^7,10,15-17, research on the ecology and control of sandflies in areas where ACL is endemic shows that human dwellings are usually located close to areas of vegetation. In endemic areas, lack of sanitation and peridomestic occupation can attract sandflies and create breeding sites for these insects^12,15,18-21, hence, the importance of studying the ecology, behavior, and development of alternative ways to control sandflies. The objectives of this study were to investigate the fauna; seasonality; and frequency of sandflies in houses, peridomestic animal shelters, and in the forest. No ACL has been recorded in the area of study, and the area is clean, well-kept, and maintained.

METHODS

The study was carried out in Santa Juliana Farm (Figure 1), located at 23° 30'21" S and 51º 54'14" W, at an altitude of 535m, and with an area of 169.4 hectares in the municipality of Sarandi in North-Central Paraná.

According to the 2000 Census, Sarandi has a population of 71,422 inhabitants - 1,929 of these are residing in rural areas and 69,493 in the urban area²².

The predominant climate in the region, according to the Köppen classification, is Cfa (humid subtropical) in which the mean temperature of the coldest month is below 18ºC and the mean annual temperatures are above 20ºC.

The mean temperature in the collection period from November 2007 to November 2008 was 23.5ºC. The lowest temperature recorded in the period was in 2008 (13.1ºC), and the highest was in 2007 (30.9ºC). The mean monthly precipitation during this same period was 130mm; the lowest rainfall for the period was 8mm in July 2008, and the highest was 235mm in December 2007. The rainfall data were provided by the Climatological Station of the Universidade Estadual de Maringá (UEM).

The region has a basaltic lithology, with a high proportion of clay in its constitution, and the soils are red oxisols (ferric) and alfisols (ferric)^23,24. The vegetation includes remnants of native semideciduous submontane forest²³.

Santa Juliana Farm contains 50.8ha of forest, of which 34.3ha is in legal reserves, and a permanent preserve of 16.5ha, where there is still a mammal fauna remaining (rodents, capybaras, wild cats, etc.) The farm has a small population of domestic animals (dogs, pigs, chickens) around the homes and cattle in the vicinity.

The study was conducted in this farm because there is no record of cases of ACL in this area. The organization of peridomicile distinguishes it from other locations in the state of Paraná where surveys of phlebotomines have been carried out^12,25,26 and the cleanliness and good organization of the farm are evident.

Sandflies were collected with Falcão light traps, twice a month from 22:00 to 02:00 hours, from November 2007 to November 2008. This resulted in a total of 104h per trap collection and 728h in total.

The traps were installed in the following ecotypes: E1 - a pigsty (Pi) with a roof and beaten earth floor, cleaned regularly, and housing two pigs; E2 - on the porch of the farm keeper's residence (R1), with a beaten earth floor, where several bags containing food were stored and 2-5 dogs rested at night, as well as several nearby trees where chickens roosted at night; E3 - on the porch of the residence (R2) of the owner of the farm, which was frequently cleaned, the grass trimmed, and the peridomestic area always dry; E4 - on the edge of the forest beside a country road; E5 - in dense forest, 25m from the edge; E6 - on the shore of a lake, with grass and fruit trees, where the residents sometimes fish; and E7 - a grassy space between trees on the shore of another lake (Figure 1).

In the extra-forest environment, traps were installed in domiciliary areas (E1, E2, and E3). The forest environment refers to the traps installed in the forest and the lakeside (E4, E5, E6, and E7).

The sandflies collected were killed with chloroform and placed in small cardboard boxes impregnated with naphthalene. The specimens were prepared and subsequently identified in the Laboratory of Parasitology, Department of Basic Health Sciences of UEM. The nomenclature used here follows Galati²⁷.

Statistical analysis was performed with data for Nyssomyia whitmani, which was collected in the largest numbers and because it is the most important species in the epidemiology of leishmaniasis in Paraná^11,28. The Chi-square test was done at a significance level of 5%, using the application Statistica 7.1.

RESULTS

A total of 4,506 sandflies were collected, belonging to the species Brumptomyia brumpti (Larrousse), Brumptomyia cunhai (Mangabeira), Evandromyia correalimai (Martins, Coutinho, & Luz), Evandromyia cortelezzii (Brèthes), Expapillata firmatoi (Barretto, Martins, & Pellegrino), Micropygomyia ferreirana (Barreto, Martins, & Pellegrino), Migonemyia migonei (France), Nyssomyia neivai (Pinto), Ny. whitmani (Antunes & Coutinho), Pintomyia fischeri (Pinto), Pintomyia monticola (Costa Lima), Pintomyia pessoai (Coutinho & Barreto), and Psathyromyia shannoni (Dyar). Of the total number of sandflies, 71.8% were Ny. whitmani, 9% were Pi. pessoai, 5.3% were Mi. migonei, 4.4% were Pi. fischeri, and 4.1% were Pi. monticola (Table 1). Altogether, these species represented 97.7% of the sandflies collected.

Table 1

We collected 2,765 females and 1,741 males. The number of female Ny. whitmani was significantly higher than the number of males of the same species (p<0.0001).

We collected a larger number of sandflies in the forest (52.6%) than in the extra-forest environments (47.4%). However, the number of specimens of Ny. whitmani was higher (p<0.0001) in the extra-forest (38.3%) compared with the forest (33.5%).

The largest numbers of sandflies in E1 (79.9%) were collected in January, March, September, and November. In E2, 74.1% of the sandflies were collected in February, May, and September. In E3, 73% of the sandflies were collected in February, March, May, and September. In E4, 77.8% of the sandflies were collected in November 2007 and January, May, July, September, and November 2008. In E5, 71.9% of the sandflies were collected in January, May, and September (Table 2). Note that in all the ecotopes together, in January, February, March, May, September, and November 2008, 82.1% of the sandflies were collected (Table 2 and Figure 2).

DISCUSSION

The 13 species collected have been recorded in several locations in the State of Paraná^11,29.30. We note particularly the species Ny. whitmani, Ny. neivai, Pi. pessoai, and Mi. migonei because of their high frequency in domiciliar and peridomiciliar situations and because they have been found naturally infected with Leishmania in this state^28,31 and in other Brazilian states^17,30,32,33.

The slightly higher number of sandflies collected in the forest was probably due to environmental conditions - i.e., humidity and organic matter necessary for the development of the immature stages of sandflies - and an available blood supply for the adult females - i.e., birds and mammals. The regular distribution of rainfall throughout the year helped to maintain soil moisture. The small number of sandflies collected in the lakeshores, despite the proximity of the forest, may have been due to the installation of traps in areas with low vegetation (grass). Ny. whitmani was collected in greater numbers outside the forest. In this environment, the high proportion of sandflies collected in ecotope E2 can be explained by the presence of several dogs that rested there and some chickens that roosted in the nearby trees at night. This confirms the attractiveness of domestic animals to phlebotomines^18,19,21. Ny. whitmani is anthropophilic³⁴ and is important in the epidemiology of ACL.

The forest preserve, the presence of wild mammals, as well as the cleanliness and organization and the small supply of blood available in the peridomicile (domestic animals) are factors that may explain the collection of similar numbers of sandflies in the forest and extra-forest areas in Santa Juliana Farm. These insects have often been collected in larger numbers in peridomiciliar and extra-forest environments^12,35,36. In Palmital Farm in the municipality of Terra Boa, Paraná, after deactivation of a colony of houses and the absence of residents and domestic animals (dogs, chickens, pigs, and others), which had served as sources of blood for the sandflies, the sandfly population decreased sevenfold³⁷. In Santa Juliana Farm, we also observed the absence of garbage and other waste in the vicinity of the houses and in the edge of the forest³⁷.

During the months of collection, the lowest mean temperatures occurred in May and June, and the lowest rainfall rates were observed in June and July. However, rainfall was well distributed throughout the collection period, and the mean, minimum, and maximum temperatures remained roughly constant. Most (65.1%) sandflies were collected in January, February, March, September, and November 2008, months that were warmer and with regular rainfall. In May, 17% of the specimens were collected, at a time when the temperature is usually milder. The finding of the highest densities of sandflies in the warmer months and with regular rainfall concords with observations in several previous surveys of these insects^36,38-42.

This study demonstrates the importance of maintaining the household and peridomestic environment clean and organized to limit the growth of the sandfly population in these environments. Having collected a large number of sandflies on the porch of one of the residences, due to the presence of domestic animals (dogs and chickens), it is recommended that separate shelters for the animals be constructed at a distance of approximately 100m from domiciles²⁵, to prevent the invasion of sandflies. Cases of leishmaniasis have been reported in locations where environmental characteristics allow the formation of the enzootic cycle of protozoans of the genus Leishmania, involving insect vectors (sandflies) and mammals (reservoirs)^11,12. In such places, sandflies have been collected in large numbers around houses and in houses that are located in close proximity to forest remnants and domestic animal shelters (chickens, pigpens, etc.), where hygiene conditions are poor, organic matter accumulates (leaves and fallen fruit, pet droppings, and leftover food offered to them), soil moisture is high, and phlebotomine populations are larger^11,12,13,18. Studies on sandfly control in northern Paraná showed that after the reorganization and cleaning of household and peridomicile environment, most sandflies were attracted by the domestic animal shelters, while the number of these insects decreased in domiciles^19,21,25.

In the present study, thirteen species of sandflies were collected, with a predominance of Ny. whitmani. Most sandflies were collected in the forest; however, Ny. whitmani was most often collected in the extra-forest. In this environment, the most number of sandflies were collected in a pigsty and on the porch of a residence. The results suggest that cleaning and organization around the houses could reduce sandfly population in peridomicile. Shelters for animals must be constructed at a distance of approximately 100m from domiciles. The study farm has an area of preserved forest, with wild animals and sandflies present, hosting a combination of factors that maintain the enzootic cycle of Leishmania. Thus, vector control for Leishmania can be achieved through basic housekeeping and maintenance of an orderly environment.

ACKNOWLEDGMENTS

Mr. Antonio E.L. da Cunha and Ms. Tatjana V.H.L. da Cunha, owners of Santa Juliana Farm, for permission to conduct the assessments. Janaína S. de Freitas and João B. Kühl, technicians of the Department of Basic Health Sciences of Universidade Estadual de Maringá, for instruction and aid in the identification of sandflies. Demilson R. Santos of the Núcleo de Entomologia de Maringá, for the illustration of the Santa Juliana Farm. Henri F. Legriffon for his assistance in collecting sandflies.

CONFLICT OF INTEREST

The authors declare that there is no conflict of interest.

FINANCIAL SUPPORT

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Proc. 410550/2006-0).

Received in 27/01/2011

Accepted in 08/09/2011

• 1. Gontijo B, Carvalho MLR. Leishmaniose tegumentar americana. Rev Soc Bras Med Trop 2003; 36:71-80.
• 2. World Health Organization (WHO). Neglected tropical diseases [Internet]. WHO; 2010 [cited 2010 Jan 22] Available from: http://www.who.int/neglected_diseases/faq/en/index4.html/
• ³
  Ministério da Saúde. Casos de Leishmaniose Tegumentar Americana. Brasil, Grandes Regiões e Unidades Federadas. 1990 a 2008 [Internet]. Brasília: Secretaria de Vigilância em Saúde; 2009 [cited 2010 Jan 30]. Available from: http://portal.saude.gov.br/portal/arquivos/pdf/casos_conf_lta.pdf /.
• 4. Teodoro U, Galati EAB, Kühl JB, Lozovei AL, Barbosa OC. Controle de flebotomíneos com DDT, em área endêmica de leishmaniose tegumentar no Estado do Paraná, sul do Brasil. Braz Arch Biol Technol 1998; 41:359-364.
• 5. Marcondes CB, Nascimento JA. Avaliação da eficiência de dentametrina (K-Othrine CE) no controle de Lutzomyia longipalpis (Diptera: Psychodidae), no Município de Santa Rita, Paraíba, Brasil. Rev Soc Bras Med Trop 1993; 26:15-18.
• 6. Falcão AL, Falcão AR, Pinto CT, Gontijo CMF, Falqueto A. Effect of deltamethrin spraying on the sandfly populations in a focus of American cutaneous leishmaniasis. Mem Inst Oswaldo Cruz 1991; 86:399-404.
• 7. Deane LM, Deane MP, Alencar JE. Observações sobre o combate ao Phlebotomus longipalpis pela desinsetização domiciliária, em focos endêmicos de calazar no Ceará. Rev Bras Malariol & D Trop 1955; 7:131-141.
• 8. Alencar JE. Profilaxia do calazar no Brasil no Ceará, Brasil. Rev Inst Med Trop 1961; 3:175-180.
• 9. Alencar JE. Expansão do calazar no Brasil. Ceará Med 1983; 5:86-120.
• 10. Alexander B, Maroli M. Control of Phlebotomine Sandflies. Med Vet Entomol 2003; 17:1-18.
• 11. 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 y Vec 2004; 11:673-680.
• 12. Teodoro U, Silveira TGV, Santos DR, Santos ES, Santos AR, Oliveira O, et al. Freqüência da fauna de flebotomíneos no domicílio e em abrigos de animais domésticos no peridomicílio, nos municípios de Cianorte e Doutor Camargo, Estado do Paraná - Brasil. Rev Patol Trop 2001; 30:209-233.
• 13. Lima AP, Minelli L, Comunello E, Teodoro U. Distribuição da leishmaniose tegumentar por imagens de sensoreamento remoto orbital, no Estado do Paraná, Sul do Brasil. An Bras Dermatol 2002; 77:681-692.
• 14. Monteiro WM, Neitzke HC, Silveira TGV, Lonardoni MVC, Teodoro U, Ferreira MEMC. Pólos de produção de leishmaniose tegumentar americana no norte do Estado do Paraná, Brasil. Cad Saúde Pública 2009; 25:1083-1092.
• 15. Barbosa MGV, Fé NF, Marcião AHR, Silva APT, Monteiro WM, Guerra JAO. Fauna de flebotomíneos (Diptera: Psychodidae) em um foco de leishmaniose tegumentar americana na área periurbana de Manaus, estado do Amazonas. Rev Soc Bras Med Trop 2008; 41:485-491.
• 16. Souza CF, Borges MAZ, Andrade AJ. Contribution to the Knowledge of the Phlebotomine Sand Flies Fauna (Diptera: Psychodidae) of Timóteo Municipality, Minas Gerais, Brazil. Neotrop Entomol 2009; 38:267-327.
• 17. 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; 103:1093-1097.
• 18. Reinhold-Castro KR, Scodro RBL, Dias-Sversutti AC, Neitzke HC, Rossi RM, Kühl JB, et al. Avaliação de medidas de controle de flebotomíneos. Rev Soc Bras Med Trop 2008; 41:269-276.
• 19. Teodoro U, Silveira TGV, Santos DR, Santos ES, Santos AR, Oliveira O, et al. Influência da reorganização, da limpeza do peridomicílio e da desinsetização de edificações na densidade populacional de flebotomíneos, no município de Doutor Camargo, Estado do Paraná, Brasil. Cad Saude Publica 2003; 19:1801-1813.
• 20. Teodoro U, Thomaz-Soccol V, Kühl JB, Santos DR, Santos ES, Santos AR, et al. Reorganization and cleaness of peridomiciliar area to control sand flies (Diptera, Psychodidae, Phlebotominae) in South Brazil. Braz Arch Biol Technol 2004; 47:205-212.
• 21. Teodoro U, Santos DR, Santos AR, Oliveira O, Poiani LP, Kühl JB, et al. Avaliação de medidas de controle de flebotomíneos no norte do Estado do Paraná, Brasil. Cad Saude Publica 2007; 23:2597-2604.
• 22. Instituto Brasileiro de Geografia e Estatística (IBGE,). Censo Demográfico de 2000 [Internet]. IBGE; 2000 cited 2011 Nov 04]. Available from: http://goo.gl/kL8jN
• ²³
  Instituto Brasileiro de Geografia e Estatística (IBGE). Mapa de Vegetação do Brasil. Brasília: IBGE. Diretoria de Geociências; 1993.
• ²⁴
  Empresa Brasileira de Pesquisa Agropecuária. (EMBRAPA). Sistema Brasileiro de Classificação de Solos. Rio de Janeiro: Centro de Pesquisas de Solos. Embrapa Solos; 1999.
• 25. Teodoro U, Kühl JB. Interação flebotomíneos, animais domésticos e dominância de Lutzomyia (Nyssomyia) intermedia (Lutz & Neiva, 1912) em área com alto grau de antropia, no Sul do Brasil. Rev Saude Publica 1997; 31:512-516.
• 26. Teodoro U, Kühl JB, Thomaz-Soccol V, Barbosa OC, Ferreira MEMC, Lozovei AL, et al. Environmental sanitation and peridomiciliar organization as auxiliary practices for the control of phlebotomines in Paraná State, Southern Brazil. Braz Arch Biol Technol 1999; 42:307-314.
• 27. Galati EAB. Morfologia e taxonomia. In: Rangel EF, Lainson R, editors. Flebotomíneos do Brasil. Rio de Janeiro: Fundação Oswaldo Cruz; 2003. p.23-51.
• 28. Luz E, Membrive N, Castro EA, Dereure J, Pratlong J, Dedet A, et al. Lutzomyia whitmani (Diptera;Ppsychodidae) as vector of Leishmania (V.) braziliensis in Paraná state, southern Brazil. Ann Trop Med Parasitol 2000; 94:623-631.
• 29. Silva AM, Camargo NJ, Santos DR, Massafera R, Ferreira AC, Postai C, et al. Diversidade, distribuição e abundância de flebotomíneos (Diptera: Psychodidae) no Paraná. Neotrop Entomol 2008; 37:209-225.
• 30. Andrade Filho JD, Galati EAB, Falcão AL. Nyssomyia intermedia (Lutz & Neiva, 1912) and Nyssomya neivai (Pinto, 1926) (Diptera: Psychodidae: Phlebotominae) geographical distribution and epidemiological importance. Mem Inst Oswaldo Cruz 2007; 102:481-487.
• 31. Oliveira DM, Reinhold-Castro KR, Bernal MVZ, Legriffon CMO, Lonardoni MVC, Teodoro U, et al. Natural infection of Nyssomyia neivai by Leishmania (Viannia) spp. in the state of Paraná, southern Brazil, detected by multiplex polymerase chain reaction. Vector-Borne Zoonotic Dis 2011; 11:137-143.
• 32. Azevedo ACR, Rangel EF, Costa EM, David J, Vasconcelos AW, Lopes UG. Natural infection of L. (Nyssomyia) whitmani (Antunes & Coutinho, 1939) by Leishmania of the braziliensis complex in Baturité, Ceará State, Northeastern Brazil. Mem Inst Oswaldo Cruz 1990a; 85:251.
• 33. Forattini OP, Pattoli DGB, Rabello EX, Ferreira AO. Infecção natural de flebotomíneos em foco enzoótico de Leishmaniose tegumentar no Estado de São Paulo. Rev Saude Publica 1972; 6:431-433.
• 34. Marcondes CB. Flebotomíneos. In: Marcondes CB, editor. Entomologia Médica e Veterinária. São Paulo: Editora Atheneu; 2001. p 34.
• 35. Teodoro U, Filho VLS, Lima EM, Misuta NM, Verginassi TG, Ferreira MEMC, et al. Leishmaniose tegumentar americana: flebotomíneos de área de transmissão no Norte do Paraná, Brasil. Rev Saude Publica 1991; 25:129-133.
• 36. Massafera R, Silva AM, Carvalho AP, Santos DR, Galati EAB, Teodoro U. Fauna de flebotomíneos do município de Bandeirantes, no Estado do Paraná. Rev Saude Publica 2005; 39:571-577.
• 37. Teodoro U, Salvia Filho VL, Lima EM, Spinosa RP, Barbosa OC, Ferreira MEMC, et al. Flebotomíneos em área de transmissão de leishmaniose tegumentar na região norte do Estado de Paraná - Brasil: Variação Sazonal e Noturna. Rev Saude Publica 1993; 27:190-194.
• 38. Teodoro U, Filho VLS, Lima EM, Spinosa RP, Barbosa OC, Ferreira MEMC, et al. Observações sobre o comportamento de flebotomíneos em ecótopos florestais e extraflorestais, em área endêmica de leishmaniose tegumentar americana, no norte do Estado do Paraná, sul do Brasil. Rev Saude Publica 1993; 27:242-249.
• 39. Teodoro U. Características ecológicas de flebotomíneos (Díptera, Psychodidae) em habitats antrópicos, município de Jussara, Paraná, Brasil [Tese de Mestrado]. Rev Soc Bras Med Trop 1996; 29:625-626.
• 40. Teodoro U, Alberton D, Kühl JB, Santos ES, Santos DR, Santos AR, et al. Ecologia de Lutzomyia (Nyssomyia) whitmani em área urbana do município de Maringá, Paraná. Rev Saude Publica 2003; 37:651-656.
• 41. Forattini OP. Novas observações sobre a biologia de flebótomos em condições naturais (Diptera, Psychodidade). Arq Hig Saude Publica 1960; 25:209-215.
• 42. Monteiro EM, Silva JCF, Costa RT, Costa DC, Barata RA, Paula EV, et al. Leishmaniose visceral: estudo de flebotomíneos e infecção canina em Montes Claros, Minas Gerais. Rev Soc Bras Med Trop 2005; 38:147-152.

Publication Dates

• Publication in this collection
  27 Feb 2012
• Date of issue
  Feb 2012