Study of Phlebotomine Sand Flies (Diptera: Psychodidae) Collected in a Leishmania-Endemic Area of the Metropolitan Region of Belo Horizonte, Brazil

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1 SAMPLING, DISTRIBUTION, DISPERSAL Study of Phlebotomine Sand Flies (Diptera: Psychodidae) Collected in a Leishmania-Endemic Area of the Metropolitan Region of Belo Horizonte, Brazil GUSTAVO M. L. CARVALHO, CÉLIA M. F. GONTIJO, ALDA L. FALCÃO, AND JOSÉ D. ANDRADE FILHO 1 Laboratório de Leishmanioses, Instituto René Rachou-Fiocruz, Av. Augusto de Lima 1715, CEP Belo Horizonte, MG, Brazil J. Med. Entomol. 47(6): 972Ð976 (2010); DOI: /ME09127 ABSTRACT Phlebotomine sand ßies are distributed across nearly all faunal regions of the world, represented by over 800 species, of which many are important vectors of human pathogens. Brazil is currently faced with the expansion and urbanization of leishmaniases, with an increase in the numbers of human cases and seropositive dogs in various medium-sized to large cities. The objective of the current study was to survey the phlebotomine sand ßy species in an area endemic for American cutaneous leishmaniasis (ACL) and American visceral leishmaniasis (AVL), i.e., the municipal district of Santa Luzia, lying within the metropolitan region of Belo Horizonte in the Brazilian State of Minas Gerais. Sand ßies were collected monthly in 2004Ð2005 using modiþed Falcão light traps hung in the peridomiciles of houses and surrounding wooded areas in the district of Baronesa. A total of 1,552 sand ßies belonging to seven species was collected, and an interesting pattern of the distribution of the most abundant species relative to the sampling locality was revealed. In the wooded areas Lutzomyia whitmani (Antunes & Coutinho) predominated, whereas in the urban area Lutzomyia longipalpis (Lutz & Neiva) was the most abundant species. These results indicate two possible epidemiological patterns of Leishmania transmission in Santa Luzia: one for American cutaneous leishmaniasis associated predominantly with wooded areas, and another for AVL, with transmission principally occurring around human habitations. KEY WORDS leishmaniasis, Minas Gerais, Phlebotominae, sand ßies Brazil is currently faced with the expansion and urbanization of both American cutaneous leishmaniasis (ACL) and American visceral leishmaniasis (AVL), with increasing numbers of Leishmania infantum chagasi infections in humans and dogs in many mediumsized and large cities. Although all Leishmania transmission in Brazil was originally conþned to rural environments, today it represents a severe public health problem in urban centers (Gontijo and Melo 2004). Leishmaniasis is currently one of the biggest public health problems of the Brazilian state of Minas Gerais. In the metropolitan region of Belo Horizonte, autochthonous cases of ACL and AVL have been recorded by health authorities since 1987 and 1989, respectively (Genaro et al. 1990, Passos et al. 1996). In Santa Luzia, a municipality within the metropolitan region of Belo Horizonte, 99 cases of ACL and 252 of AVL were reported between 2000 and 2007 (SINAN 2008). 1 Corresponding author: Laboratório de Leishmanioses, Instituto René Rachou-Fiocruz, Avenida Augusto de Lima 1715, CEP , Belo Horizonte, MG, Brazil ( jandrade@cpqrr.þocruz.br). Phlebotomine sand ßies are distributed across nearly all faunal regions of the world, with many species considered to be important vectors of Leishmania based on epidemiological and/or experimental data. However, relatively few species have been identiþed as primary vectors, based on degree of anthropophily, natural infection, and spatial distribution overlapping that of the disease (Rangel and Lainson 2003). It is therefore important to know about the phlebotomine fauna in urban foci of leishmaniasis. The identiþcation of potential vectors within these foci is fundamental, each species presenting distinct biological and ecological characteristics that should be taken into account in the implementation of vector control measures. The objective of the present work was to study the phlebotomine sand ßy fauna of a Leishmania-endemic area, i.e., the municipal district of Santa Luzia in Greater Belo Horizonte, state capital of Minas Gerais, Brazil. Materials and Methods The municipality of Santa Luzia occupies an area of 235 km 2 with 219,699 inhabitants (IBGE 2006). The /10/0972Ð0976$04.00/ Entomological Society of America

2 November 2010 CARVALHO ET AL.: SAND FLIES IN AN ENDEMIC AREA OF MINAS GERAIS 973 Table 1. Distribution by month and sex of the sand flies collected between November (2004) and October (2005) in the district of Baronesa, Santa Luzia/MG Months Species Nov. Dec. Jan. Feb. Mar. April May June July Aug. Sept. Oct. Total Lu. longipalpis Lu. whitmani Lu. pessoai Lu. intermedia Lu. cortelezzii Lu. oliveirai Lu. neivai Lutzomyia sp Total ,277 current study was conducted between November 2004 and October 2005 in the urban district of Baronesa, which retains some rural characteristics and has previously reported autochthonous cases of human infection with Leishmania. Serological studies have revealed a high prevalence of positive dogs in the area (Diretoria de Ações Descentralizadas de Saúde de Belo Horizonte, unpublished data). Sand ßies were collected monthly using modiþed light traps (Falcão 1981) hung in speciþc areas in which the insects would most likely be found, such as dog kennels, henhouses, pigsties, and areas with vegetation. The light traps were switched on during the hours of darkness (18:00Ð06:00). Seventeen traps were used, 14 of them in the peridomiciles of houses, and three in a wooded area with vegetation on the margin of the district. All sand ßies collected were prepared and slide mounted in BerleseÕs ßuid or Canada balsam. The insects were identiþed based on the keys of Young and Duncan (1994). The voucher species were deposited in the phlebotomine sand ßy collection of the Centro de Pesquisas René Rachou/Fiocruz. Climatological data (temperature, humidity, and rainfall) were obtained from the Controle de Zoonosis of Belo Horizonte (MG, Brazil). Sand ßy density was correlated with climatic data using SpearmanÕs rank correlation coefþcient. Results A total of 1,277 phlebotomine sand ßy specimens was collected in the light traps, of which 307 (24%) were females and 970 (76%) males. The distribution of species captured by month and sex is shown in Table 1. The following species were captured: Lutzomyia longipalpis (Lutz & Neiva), Lutzomyia intermedia (Lutz & Neiva), Lutzomyia whitmani (Antunes & Coutinho), Lutzomyia pessoai (Coutinho & Barreto), Lutzomyia cortelezzii (Brethes), Lutzomyia neivai (Pinto), and Lutzomyia oliveirai (Martins, Silva & Falcão). Another Lutzomyia sp. present in the collections could not be identiþed because the specimens were damaged. The species Lu. whitmani represented 75% of the total of specimens of phlebotomines captured in the study area, followed by Lu. longipalpis, with 19% of the total (Fig. 1). Although the number of traps was lower in the wooded area than in the urban one, collections from the former area represented 77.8% of the total samples collected. The ratio of phlebotomine sand ßies/trap for the period sampled was 311:1 in the wooded area and 20:1 in the urban area. Although Lu. whitmani was more abundant overall than Lu. longipalpis, when the two species were compared separately for the two habitats, a statistically signiþcant difference was revealed (P 0.05; Fig. 2), with Lu. whitmani predominating in the wooded area and Lu. longipalpis more abundant around houses. Although the largest numbers of sand ßies were collected during the month of October, there was no statistically signiþcant correlation between the total density of sand ßies and any of the climatic variables (Table 2, Fig. 3). Fig. 1. Relative abundance of sand ßy species collected in the district of Baronesa, Santa Luzia/MG, November 2004 to October Fig. 2. Statistical comparison of distributions of Lu. longipalpis and Lu. whitmani according to area of capture in the urban district of Baronesa, Santa Luzia/MG, November 2004 to October 2005.

3 974 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 47, no. 6 Table 2. Correlation between the total density of phlebotomine sand flies collected between November 2004 and October 2005 in the urban district of Baronesa, Santa Luzia municipality, Minas Gerais State, and climatic variables Total density of phlebotomine sand ßies Climatic variables Temperature Humidity Rainfall 0.035(*) 0.336(*) 0.175(*) Correlation coefþcient P value * Correlation not signiþcant at P Discussion As in several other Brazilian cities, the unplanned growth of the municipal district of Santa Luzia has been associated with increasing problems of public health, resulting in drastic environmental transformations and allowing the Leishmania transmission cycle to become established. The transmission of Leishmania spp. involves different species of phlebotomine sand ßy in close association with parasites and reservoirs (Rangel and Lainson 2003). Detailed serological surveys of domestic dog populations as well as sand ßy sampling surveys have revealed high prevalence of infections in many areas associated with the predominance of certain vector species, resulting in a high risk of human exposure to Leishmania (Vieira and Coelho 1998). Rapid changes in environmental conditions in many tropical regions caused by habitat destruction, deforestation, and urbanization have had an enormous inßuence on vector populations and Leishmania transmission, favoring certain sand ßy species over others (Bejarano et al. 2002). Situations with domestic animal shelters very close to human habitations, poor hygiene conditions in the peridomicile, and close proximity to small remnants of forest are very common throughout Brazil. The urban district of Baronesa displays all of these factors, which together seem to favor the concentration of phlebotomines and mammalian reservoirs of Leishmania in the peridomicile (Gomes and Nevis 1998, Saraiva et al. 2006). There is strong evidence that the presence of domestic and wild animals in the peridomicile attracts large numbers of phlebotomines, including vectors of Leishmania sp. (Alexander 2000, Brazil et al. 1991, Barata et al. 2005, Nascimento et al. 2007). Several epidemiologically important species were collected in the urban district of Baronesa, notably Lu. longipalpis, Lu. intermedia, Lu. neivai, and Lu. whitmani. The last species has been incriminated as a vector of Leishmania braziliensis (Azevedo et al. 1990, Queiroz et al. 1994, Luz et al. 2000). The two most abundant species in this study, i.e., the Le. braziliensis vector Lu. whitmani (ACL) and the Le. chagasi infantum vector Lu. longipalpis (AVL), clearly favored different habitat types, with the former more abundant in wooded areas and the latter predominating around human habitations. Thus, it appears that two different transmission cycles are occurring within the Santa Luzia district, a sylvatic one for ACL involving Lu. whitmani and a truly urban one for AVL, as a result of biting by Lu. longipalpis. The patterns of geographical distribution of both species have been described in previous studies (Souza et al. 2004, Loyola et al. 2007, Andrade Filho et al. 2008, Paula et al. 2008, Souza and Borges 2008). It should be noted that in this area, two species have already been found naturally infected using the polymerase chain reaction technique, i.e., Lu. whitmani with Le. (Viannia) spp. and Lu. cortelezzii with Le. infantum chagasi (Carvalho et al. 2008). However, the latter Þnding is not sufþcient to incriminate Lu. cortelezzii as a vector of Le. infantum chagasi. Further studies are required on the behavior of this species, its spatial distribution in relation to AVL, and elucidation of the vector-parasite relationship (Carvalho et al. 2008). Although captured in smaller numbers in Baronesa, Lu. intermedia and Lu. neivai have been implicated in Fig. 3. Correlation of sand ßy density with monthly climatic variables between November 2004 and October 2005, district of Baronesa, Santa Luzia/MG.

4 November 2010 CARVALHO ET AL.: SAND FLIES IN AN ENDEMIC AREA OF MINAS GERAIS 975 the transmission of ACL-causing parasites in various regions of Brazil (Andrade Filho et al. 2007). The sympatric occurrence of these two species in some regions of Brazil and the great morphological similarity between them are noteworthy (Andrade Filho et al. 2003, Saraiva et al. 2008). Climatic and ecological factors are important links in the epidemiology of AVL (Sherlock 1996), but inßuence phlebotomine populations in a variety of ways. Sand ßies are usually found in greater numbers during hot and humid months (Aguiar and Soucasaux 1984, Gomes and Galati 1987). Deane and Deane (1965) investigated seasonal inßuences on Lu. longipalpis and found that the increased humidity during the rainy season directly promoted proliferation and survival of this sand ßy species. However, in the current study, no correlation was found between sand ßy abundance and environmental factors, a fact already observed by other authors (Condino et al. 1998). Although the current study focused on only one area, these Þndings will be useful considerations in selection of the most appropriate control measures by public health authorities. Further studies are needed to provide more important information for support of leishmaniasis control programs in Brazil. References Cited Aguiar, G. M., and T. Soucasaux Aspectos da ecologia dos ßebótomos do Parque Nacional da Serra dos Órgãos, Estado do Rio de Janeiro. I. Freqüência mensal em isca humana (Diptera, Psychodidae, Phlebotominae). Mem. Inst. Oswaldo Cruz 79: 179Ð209. Alexander, B Sampling methods for phlebotomine sandßies. Med. Vet. Entomol. 14: 109Ð122. Andrade Filho, J. D., E.A.B. Galati, and A. L. Falcão Redescription of Nyssomyia intermedia (Lutz & Neiva, 1912) and Nyssomyia neivai (Pinto, 1926) (Diptera: Psychodidae). 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