• View in gallery

    (A) Fine mesh, (B) wooden box, (C) metal plate, and (D) assembled trap.

  • View in gallery

    Abundance of phlebotomine sand flies collected using soil monitoring traps installed in the peridomicile at three distances from houses in a cutaneous leishmaniasis-endemic area of SE Brazil from May to October 1999.

  • View in gallery

    Phlebotomine sand flies collected in Shannon traps installed from 6:00 to 10:00 PM in the peridomiciles of houses where breeding sites were identified in a cutaneous leishmaniasis-endemic area of SE Brazil, May–September 1999.

  • 1.

    Grimaldi G, Tesh RB, McMahon-Pratt D, 1989. A review of geographical distribution and epidemiology of leishmaniasis in the New World. Am J Trop Med Hyg 41: 687725.

    • Search Google Scholar
    • Export Citation
  • 2.

    Herrer A, Christensen HA, 1976. Natural cutaneous leishmaniasis among dogs in Panamá. Am J Trop Med Hyg 25: 5963.

  • 3.

    Aguilar CM, Fernandez E, Fernandez R, Deane LM, 1984. Study of an outbreak of cutaneous leishmaniasis in Venezuela: the role of domestic animals. Mem Inst Oswaldo Cruz 79: 181195.

    • Search Google Scholar
    • Export Citation
  • 4.

    Falqueto A, Coura JR, Barros GC, Grimaldi FG, Sessa PA, Carias VR, Jesus AC, Alencar JT, 1986. Participação do cão no ciclo de transmissão da leishmaniose tegumentar no município de Viana, Estado do Espírito Santo, Brasil. Mem Inst Oswaldo Cruz 81: 155163.

    • Search Google Scholar
    • Export Citation
  • 5.

    Herrer A, 1951. Estudio sobre leishmaniasis tegumentaria en el Peru. V. Leishmaniasis natural em perros procedentes de localidades utógenas. Rev Med Exp 8: 87117.

    • Search Google Scholar
    • Export Citation
  • 6.

    Mazza S, 1927. Leishmaniose cutánea en el caballo y nueva observacion de la misma en el perro. Bol Inst Clin Quir 3: 462464.

  • 7.

    Barros GC, Sessa PA, Mattos EA, Carias VR, Mayrink W, Alencar JT, Falqueto A, Jesus AC, 1985. Foco de leishmaniose tegumentar americana nos municípios de Viana e Cariacica, Estado do Espírito Santo, Brasil. Rev Saude Publica 19: 146153.

    • Search Google Scholar
    • Export Citation
  • 8.

    Lima WS, Dias M, Costa CA, Nogueira RH, Michalick MS, Falqueto A, 1986. Histopatologia e terapêutica da leishmaniose tegumentar canina, naturalmente adquirida. Rev Bras Med Vet Zootec 38: 3341.

    • Search Google Scholar
    • Export Citation
  • 9.

    Aguilar CM, Rangel EF, Garcia L, Fernandez E, Momen H, Grimaldi FG, Vargas Z, 1989. Zoonotic cutaneous leishmaniasis due to Leishmania (Viannia) braziliensis associated with domestic animals in Venezuela and Brazil. Mem Inst Oswaldo Cruz 84: 1928.

    • Search Google Scholar
    • Export Citation
  • 10.

    Falqueto A, Sessa PA, Varejão JB, Barros GC, Momem H, Grimaldi G Jr, 1991. Leishmaniasis due to Leishmania braziliensis in Espirito Santo state: further evidence on the role of dogs as a reservoir of infection for humans. Mem Inst Oswaldo Cruz 86: 499500.

    • Search Google Scholar
    • Export Citation
  • 11.

    Cunha JC, Lima JW, Pompeu MM, 2006. Transmissão domiciliar de leishmaniose tegumentar e associação entre leishmaniose humana e canina, durante uma epidemia na Serra do Baturité, no estado do Ceará, Brasil. Rev Bras Epidemiol 9: 425435.

    • Search Google Scholar
    • Export Citation
  • 12.

    Oliveira-Neto MP, Pirmez C, Rangel E, Schubach A, Grimaldi G Jr, 1988. An outbreak of american cutaneous leishmaniasis (Leishmania braziliensis braziliensis) in a periurban area of Rio de Janeiro city, Brazil: clinical and epidemiological studies. Mem Inst Oswaldo Cruz 83: 427435.

    • Search Google Scholar
    • Export Citation
  • 13.

    Rangel EF, Azevedo AC, Andrade CA, Souza NA, Wermelinger ED, 1990. Studies on sand fly fauna (Diptera: Psychodidae) in a foci of cutaneous leishmaniasis in Mesquita, Rio de Janeiro state, Brazil. Mem Inst Oswaldo Cruz 85: 3945.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ferreira AL, Sessa PA, Varejão JB, Falqueto A, 2001. Distribution of sand flies (Diptera: Psychodidae) at different altitudes in an endemic region of american cutaneous leishmaniasis in the State of Espírito Santo, Brazil. Mem Inst Oswaldo Cruz 96: 10611067.

    • Search Google Scholar
    • Export Citation
  • 15.

    Alexander B, de Oliveria EB, Haigh E, de Almeida LL, 2002. Cutaneous leishmaniasis in coffee plantations of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 97: 627630.

    • Search Google Scholar
    • Export Citation
  • 16.

    Coutinho JO, Barreto MP, 1941. Dados bionômicos sobre o Phlebotomus fischeri Pinto, 1926 (Diptera, Psychodidae). Rev Bras Biol 1: 423429.

    • Search Google Scholar
    • Export Citation
  • 17.

    Alencar RB, 2007. Emergência de flebotomíneos (Diptera: Psychodidae) em chão de floresta de terra firme na Amazônia Central do Brasil: Uso de um modelo modificado de armadilha de emergência. Acta Amazon 37: 287292.

    • Search Google Scholar
    • Export Citation
  • 18.

    Arias JR, Freitas RA, 1982. On the vectors of cutaneous leishmaniasis in the Central Amazon of Brazil. 4. Sand fly emergence from a “terra firme” forest floor. Acta Amazon 12: 609611.

    • Search Google Scholar
    • Export Citation
  • 19.

    Bettini S, Contini C, Atzeni MC, Tocco G, 1986. Leishmaniasis in Sardinia. I. Observations on a larval breeding site of Phlebotomus perniciosus, Phlebotomus perfiliewi perfiliewi and Sergentomyia minuta (Diptera: Psychodidae) in the canine leishmaniasis focus of Soleminis (Cagliari). Ann Trop Med Parasitol 80: 307315.

    • Search Google Scholar
    • Export Citation
  • 20.

    Doha S, Kamal H, Shehata M, Helmy N, Kader MA, El Said S, El Sawaf BM, 1990. The breeding habitats of Phlebotomus sand flies (Diptera: Psychodidae) in Al Agamy, Alexandria, Egypt. J Egypt Soc Parasitol 20: 747752.

    • Search Google Scholar
    • Export Citation
  • 21.

    Feliciangeli MD, 2004. Natural breeding places of phebotomine sandflies. Med Vet Entomol 18: 7180.

  • 22.

    Pifano CF, 1941. La leishmaniosis tegumentaria en el estado Yaracuy, Venezuela. Gac Med Caracas 48: 292299.

  • 23.

    Forattini OP, 1954. Algumas observações sobre biologia de flebótomos (Diptera, Psychodidae) em região da bacia do rio Paraná (Brasil). Arq Fac Hig Saúde Públ 8: 15136.

    • Search Google Scholar
    • Export Citation
  • 24.

    Forattini OP, 1960. Novas observações sobre a biologia de flebótomos em condições naturais (Diptera, Psychodidae). Arq Fac Hig Saúde Públ 25: 209215.

    • Search Google Scholar
    • Export Citation
  • 25.

    Ferro C, Pardo R, Torres M, Morrison A, 1997. Larval microhabitats of Lutzomyia longipalpis (Diptera: Psychodidae) in a endemic focus of visceral leishmaniasis in Colombia. J Med Entomol 34: 719728.

    • Search Google Scholar
    • Export Citation
  • 26.

    Casanova C, 2001. A soil emergence trap for collections of phlebotomine sand flies. Mem Inst Oswaldo Cruz 96: 273275.

  • 27.

    Deane LM, Deane MP, 1957. Observações sobre abrigos e criadouros de flebótomos no noroeste do Estado do Ceará. Rev Bras Malariol Doencas Trop 9: 225246.

    • Search Google Scholar
    • Export Citation
  • 28.

    Oliveira CD, Assunção RM, Reis IA, Proietti FA, 2001. Spatial distribution of human and canine visceral leishmaniasis in Belo Horizonte, Minas Gerais State, Brasil, 1994–1997. Cad Saude Publica 17: 12311239.

    • Search Google Scholar
    • Export Citation
  • 29.

    Costa CH, Tapety CM, Werneck GL, 2007. Controle da leishmaniose visceral em meio urbano: estudo de intervenção randomizado fatorial. Rev Soc Bras Med Trop 40: 415419.

    • Search Google Scholar
    • Export Citation
  • 30.

    Werneck GL, 2008. Forum: geographic spread and urbanization of visceral leishmaniasis in Brazil. Introduction. Cad Saude Publica 24: 29372940.

    • Search Google Scholar
    • Export Citation
  • 31.

    Costa CH, Pereira HF, Araújo MV, 1990. Epidemia de leishmaniose visceral no estado do Piauí, Brasil, 1980–1986*. Rev Saude Publica 24: 361372.

    • Search Google Scholar
    • Export Citation
  • 32.

    Disney RH, 1966. A trap for phlebotomine sandflies attracted to rats. Bull Entomol Res 56: 445451.

  • 33.

    Peel MC, Finlayson BL, McMahon TA, 2007. Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11: 16331644.

  • 34.

    Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A, 2005. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25: 19651978.

    • Search Google Scholar
    • Export Citation
  • 35.

    Shannon R, 1939. Methods for colleting and feeding mosquitoes in jungle yellow fever studies. Am J Trop Med Hyg 19: 131140.

  • 36.

    Young DG, Duncan MA, 1994. Guide to the Identification and Geographic Distribuition of Lutzomyia Sand Flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae). Gainesville, FL: Associated Publishers of the American Entomological Institute.

    • Search Google Scholar
    • Export Citation
  • 37.

    Camargo-Neves VL, Gomes AC, Antunes JL, 2002. Correlação da presença de espécies de flebotomíneos (Diptera: Psychodidae) com registros de casos da leishmaniose tegumentar americana no Estado de São Paulo, Brasil. Rev Soc Bras Med Trop 35: 299306.

    • Search Google Scholar
    • Export Citation
  • 38.

    Rangel EF, Souza NA, Wermelinger ED, Barbosa AF, 1984. Infecção natural de Lutzomyia intermedia Lutz & Neiva 1912, em área endêmica de leishmaniose tegumentar no Estado do Rio de Janeiro. Mem Inst Oswaldo Cruz 79: 395396.

    • Search Google Scholar
    • Export Citation
  • 39.

    Azevedo AC, Rangel EF, Queiroz RG, 1990. Lutzomyia migonei (França, 1920) naturally infected with peripylarian flagellates in Baturité, a focus of cutaneous leishmaniasis in Ceará State, Brazil. Mem Inst Oswaldo Cruz 85: 479.

    • Search Google Scholar
    • Export Citation
  • 40.

    Falqueto A, Varejão JB, Sessa PA, 1987. Cutaneous leishmaniasis in a horse (Equus caballus) from endemic area in the state of Espírito Santo, Brazil. Mem Inst Oswaldo Cruz 82: 443.

    • Search Google Scholar
    • Export Citation
  • 41.

    Dougherty MJ, Guerin PM, Ward RD, 1994. Isolation of oviposition pheromone from the eggs of the sandfly Lutzomyia longipalpis. Med Vet Entomol 8: 119124.

    • Search Google Scholar
    • Export Citation
  • 42.

    Dougherty MJ, Guerin PM, Ward RD, 1995. Identification of oviposition attractants for the sandfly Lutzomyia longipalpis (Diptera: Psychodidae) in volatiles of feces from vertebrates. Physiol Entomol 20: 2332.

    • Search Google Scholar
    • Export Citation
  • 43.

    Pita-Pereira D, Souza GD, Pereira TA, Zwetsch A, Britto C, Rangel EF, 2011. Lutzomyia (Pintomyia) fischeri (Diptera: Psychodidae: Phlebotominae), a probable vector of American cutaneous leishmaniasis: detection of natural infection by Leishmania (Viannia) DNA in specimens from the municipality of Porto Alegre (RS), Brazil, using multiplex PCR assay. Acta Trop 120: 273275.

    • Search Google Scholar
    • Export Citation
  • 44.

    Rocha LS, Falqueto A, Santos CB, Ferreira AL, Graça GC, Grimaldi G Jr, Cupolillo E, 2010. Survey of natural infection by Leishmania in sand fly species collected in southeastern Brazil. Trans R Soc Trop Med Hyg 104: 461466.

    • Search Google Scholar
    • Export Citation
  • 45.

    Alexander B, Maroli M, 2003. Control of phlebotomine sandflies. Med Vet Entomol 17: 118.

  • 46.

    Falcão AL, Falcão AR, Pinto CT, Contijo CM, Falqueto A, 1991. Effect of deltamethrin spraying on the sandfly populations in a focus of american cutaneous leishmaniasis. Mem Inst Oswaldo Cruz 86: 399404.

    • Search Google Scholar
    • Export Citation
  • 47.

    Teodoro U, Thomaz-Soccol V, Kühl JB, Santos DR, Santos ES, Santos AR, Abbas M, Dias AC, 2004. Reorganization and cleanness of peridomiciliar area to control sand flies (Diptera, Psychodidae, Phlebotominae) in South Brazil. Braz Arch Biol Technol 47: 205212.

    • Search Google Scholar
    • Export Citation
  • 48.

    Teodoro U, Santos DR, Santos AR, Oliveira O, Santos ES, Neitzke HC, Monteiro WM, Rossi RM, Lonardoni MV, Silveira TG, 2006. Avaliação de medidas de controle de flebotomíneos no Município de Lobato, Estado do Paraná, Sul do Brasil. Cad Saude Publica 22: 451455.

    • Search Google Scholar
    • Export Citation
  • 49.

    Reinhold-Castro KR, Scodro RB, Dias-Sversutti AC, Neitzke HC, Rossi RM, Kühl JB, Silveira TGV, Teodoro U, 2008. Avaliação de medidas de controle de flebotomíneos. Rev Soc Bras Med Trop 41: 269276.

    • Search Google Scholar
    • Export Citation

 

 

 

 

 

Peridomiciliary Breeding Sites of Phlebotomine Sand Flies (Diptera: Psychodidae) in an Endemic Area of American Cutaneous Leishmaniasis in Southeastern Brazil

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  • Unidade de Medicina Tropical, Universidade Federal do Espírito Santo, Vitória, Espírito Santo, Brazil

The occurrence of American cutaneous leishmaniasis (ACL) in areas modified by humans indicates that phlebotomine sand fly vectors breed close to human habitations. Potential peridomiciliary breeding sites of phlebotomines were sampled in an area of transmission of Leishmania (Viannia) braziliensis in Southeastern Brazil. Three concentric circles rounding houses and domestic animal shelters, with radii of 20, 40, and 60 m, defined the area to be monitored using adult emergence traps. Of the 67 phlebotomines collected, Lutzomyia intermedia comprised 71.6%; Lutzomyia schreiberi, 20.9%; and Lutzomyia migonei, 4.5%. The predominance of L. intermedia, the main species suspected of transmitting L. (V.) braziliensis in Southeastern Brazil, indicates its participation in the domiciliary transmission of ACL, providing evidence that the domiciliary ACL transmission cycle might be maintained by phlebotomines that breed close to human habitations. This finding might also help in planning measures that would make the peridomiciliary environment less favorable for phlebotomine breeding sites.

Introduction

American cutaneous leishmaniasis (ACL) was originally a disease found mainly in forest habitats, occurring from the Southern United States to Argentina.1 Human infection occurs when people enter forest habitats where phlebotomine sand flies and wild mammals maintain the enzootic cycle of several species of Leishmania. The devastation of forests has altered the epidemiological characteristics of ACL throughout South and Central America.25

In areas of ancient colonization in Southeastern (SE) Brazil, the disease now occurs in peri-urban areas where the forest is not close to residences, affecting adults and children of both sexes. Dogs and horses are frequently found to be infected with Leishmania (Viannia) braziliensis,69 and the association between human and canine cutaneous leishmaniasis has already been shown in residences where people live with infected dogs4,10,11; in these areas, sand flies are found in high densities in and around houses. The most abundant species include Lutzomyia intermedia, Lutzomyia whitmani, and Lutzomyia migonei, which are considered to be the most likely vectors of L. (V.) braziliensis in SE Brazil.7,1214 Considering that human habitations are normally situated more than 300 m from forests remnants, it is possible that the insect vectors breed within the field plots of coffee and bananas that commonly surround houses in this area.15

Various studies on sand fly breeding sites focusing on the worldwide Leishmania transmission have been carried out using different techniques in areas with various levels of disturbance by human activity and in forest habitats.1621 However, in the Americas, there have been few studies on peridomiciliary breeding sites; many studies generally involve isolated collections of a few specimens.2225 In Brazil, Casanova26 detected breeding sites of L. intermedia and L. whitmani in an ACL area, whereas Deane and Deane27 identified various breeding sites of Lutzomyia longipalpis in an area of American visceral leishmaniasis (AVL) transmission, by surveying both forested and peridomiciliary habitats. In AVL areas, L. longipalpis is encountered in habitats that are completely urbanized,2831 providing an epidemiological scenario very different from that observed in ACL-endemic areas.

Thus, little is known about the breeding sites of the sand fly vectors of L. (V.) braziliensis or other species causing ACL in peridomiciliary habitats. Demonstrating the presence of breeding sites in proximity to houses, together with the presence of infected domestic animals, might suggest a scenario of domiciliary transmission of the disease independent of the sylvatic cycle of the zoonosis. The objective of this study was to investigate the occurrence of sand fly breeding sites by the systematic monitoring of soil around houses and peridomiciliary outbuildings in an ACL-endemic area of SE Brazil.

Materials

We investigated sand fly breeding sites using an adult emergence trap that was conceived and constructed on the basis of the model described by Disney32 (Figure 1). Each trap consisted of a square wooden frame placed over the soil to enclose a surface area of 0.25 m2. A metal plate with a central opening to allow the passage of adult insects was installed inside the box held 10 cm above the soil surface by four metal rods. This part was coated using a paintbrush and castor oil (Ricinus communis) to retain any sand flies that emerged within the trap. The upper part of the box was covered with fine mesh that prevented the escape of insects that had not yet touched the oiled plate. Finally, a plastic cover of dimensions 2 × 2 m protected the trap from rain.

Figure 1.
Figure 1.

(A) Fine mesh, (B) wooden box, (C) metal plate, and (D) assembled trap.

Citation: The American Society of Tropical Medicine and Hygiene 87, 6; 10.4269/ajtmh.2012.12-0470

Methods

The study was carried out in an ACL-endemic area located in the municipality of Viana (20°22′S; 40°31′W) in the SE Brazilian state of Espírito Santo, with a mean elevation of 28 m above sea level. According to the Köppen-Geiger classification, the region has a tropical monsoon climate33 with a mean annual temperature of 24°C (range 17–32°C) and an annual precipitation of ∼1,200 mm34; the area presents an irregular relief and has been colonized for more than a century. There are crops of bananas, coffee, vegetables, and fruit trees as well as remnants of the Atlantic rainforest in the parts unsuitable for agriculture, and generally situated more than 200 m away from residences. The sampled area had two houses occupied by adults and children of both sexes. The peridomicile of these houses included a pigsty, a henhouse, and an outbuilding with four stalls used to store food and agricultural materials and to function as a stable for horses. The domestic animals were principally dogs, pigs, and chickens.

The houses and domestic animal shelters were set very close together, representing the geometric center of the monitored area. Three concentric circles rounding these structures, with radii of 20, 40, and 60 m, defined the area to be monitored. The first sampling range was situated 0–20 m away from the center; the second, 20–40 m; and the third, 40–60 m. Twelve traps (four at each sampling range) were installed simultaneously, allowing for 3 m2 of soil to be monitored (1 m2 at each sampling range). To avoid accidentally collecting adult sand flies already resting in the soil, each installation was carefully swept before each sampling period.

The traps were installed in patches of shaded soil, rich in organic material and protected from wind and humidity. They were examined every 48 hr to collect sand flies. The traps were moved around weekly within the limits of each station to ensure optimum coverage of patches where sand fly breeding sites could exist.

The study was carried out from May to October 1999, which included a total of 16 weeks of monitoring. Logistic regression analysis was performed to determine whether the presence of sand fly breeding sites in the peridomicile could be predicted according to the distance from houses and domestic animal shelters. Each sampling unit was represented by the four traps installed at each station for 1 week, thereby giving a total of 48 samples (3 stations × 16 weeks).

To compare the population of recently emerged adult sand flies with those active in the area at night, five control collections were performed with two Shannon traps installed in the surrounding dwellings, away from the houses respectively 10 and 50 m from 6:00 to 10:00 PM; the insects were collected off the sides of the trap with a mouth aspirator.35 The collected sand flies were mounted on slides and identified according to the keys of Young and Duncan.36

Results

A total of 1,344 traps were installed, representing a sample effort of 336 m2 soil surface during 24 hr. A total of 67 sand flies belonging to 5 species were collected from the 3 stations, which is equivalent to an emergence rate of 19.9 sand flies × 100 m2 × day−1. Of these 67 insects, 44 (65.7%) were males and 23 (34.3%) females. Twenty-six (38.8%) were collected at the innermost station; 22 (32.8%), at the second; and 19 (28.4%), at the third (Figure 2).

Figure 2.
Figure 2.

Abundance of phlebotomine sand flies collected using soil monitoring traps installed in the peridomicile at three distances from houses in a cutaneous leishmaniasis-endemic area of SE Brazil from May to October 1999.

Citation: The American Society of Tropical Medicine and Hygiene 87, 6; 10.4269/ajtmh.2012.12-0470

The most numerous species was L. intermedia with 48 individuals (71.6%), followed by Lutzomyia schreiberi with 14 (20.9%). Lutzomyia intermedia were the most abundant at the first and second stations with 22 and 18 specimens, respectively. Lutzomyia schreiberi was the most abundant at the third station where 10 specimens were collected (Figure 2). Logistic regression analysis revealed that the probability of sand fly occurrence did not change with distance from the houses and animal shelters (degrees of freedom [df] = 1, N = 48; L. intermedia: x2 = 3.2, P = 0.08; L. schreiberi: x2 = 5.5, P = 0.02; L. migonei: x2 = 0.6, P = 0.46; Lutzomyia fischeri: x2 = 0.0, P = 1.0; Lutzomyia ferreirana: x2 = 0, P = 1.0; total: x2 = 0.2, P = 0.69).

The control collections included 5,812 sand flies of 8 species, of which 4,915 (84.6%) were males and 897 (15.4%) females. Once again, L. intermedia was the most abundant with 5,646 specimens (97.1%), followed by L. migonei with 92 (1.6%; Figure 3).

Figure 3.
Figure 3.

Phlebotomine sand flies collected in Shannon traps installed from 6:00 to 10:00 PM in the peridomiciles of houses where breeding sites were identified in a cutaneous leishmaniasis-endemic area of SE Brazil, May–September 1999.

Citation: The American Society of Tropical Medicine and Hygiene 87, 6; 10.4269/ajtmh.2012.12-0470

Discussion

Systematic monitoring of the soil surface revealed the existence of suitable sites for oviposition and the development of immature sand flies in the peridomicile.

Natural breeding sites of L. intermedia and L. whitmani have already been identified in SE Brazil in both sylvatic and peridomiciliary habitats.23,24,26 In Northeastern Brazil, Deane and Deane27 found breeding sites of L. longipalpis in the vicinity of human habitations, which explains the occurrence of this visceral leishmaniasis vector in ancient colonized areas, including urban ones. In this study, various species of sand flies, principally L. intermedia and L. migonei, which probably transmit Leishmania to humans and dogs, were found to be breeding around human habitations.14,37 These species were found to be naturally infected with L. (V.) braziliensis, thus providing further evidence of their participation in the epidemiological cycle of ACL.38,39

Several authors hypothesize the occurrence of a domiciliary transmission cycle of ACL involving humans and domestic animals, especially dogs and horses.3,4,9,12,40 The discovery of peridomiciliary breeding sites of sand fly vectors of L. (V.) braziliensis supports this hypothesis, suggesting that they are able to survive and transmit Leishmania in areas devoid of forests. Even with the number of sand flies collected being relatively low, the results were relevant; since the entire monitored area (covered by the 60 m radius) was sampled, the estimations show the emergence of more than 2,000 phlebotomine sand flies per day. This estimation predicts the maintenance of a wide population in the peridomicile, independent of forests.

The generalist behavior of L. intermedia explains its greater occurrence observed in the breeding sites. Its greater ability to reproduce around houses would explain its high density and its predominance over other species in this environment, as observed in the nocturnal collections. The homogenous occurrence of L. intermedia in samples at three different distance stations from houses and domestic animal shelters is concordant with the findings of studies that identified sand fly breeding sites in a variety of ecotopes.21,25,27 On the other hand, the present results contradict those of other studies that indicate a preference for breeding sites close to domestic animals, where adults and immatures would have greater access to food and shelter.21,23,24 Previous experiments show that female L. longipalpis searching for breeding sites are attracted by volatile compounds present in vertebrate feces and by pheromones secreted by other females onto eggs during oviposition.41,42

The presence of L. schreiberi, L. migonei, L. fischeri, and L. ferreirana in peridomiciliary breeding sites, even in small numbers, shows that these species are also able to survive in habitats modified by humans. In addition to L. intermedia, L. migonei may also be involved in the domiciliary transmission of ACL.14,37 Both L. fischeri and L. ferreirana were recently found to be infected with Leishmania (Viannia) in rural areas of SE and S Brazil where ACL is endemic.43,44

Knowledge of the peridomiciliary breeding sites of phlebotomine sand flies could help orient environmental intervention measures that would impede the breeding of these insects and justify the application of insecticides to control household transmission.45 It was found that reorganizing and cleaning of the peridomicile and the application of residual insecticides in houses and outbuildings significantly reduces sand fly populations in ACL-endemic areas modified by human activities.4649 We suggest that similar studies in areas with urban transmission of AVL be conducted, because identifying the breeding sites of L. longipalpis could enhance the planning of vector control measures.

ACKNOWLEDGMENT

We thank Bruce Alexander for carefully reviewing this manuscript.

  • 1.

    Grimaldi G, Tesh RB, McMahon-Pratt D, 1989. A review of geographical distribution and epidemiology of leishmaniasis in the New World. Am J Trop Med Hyg 41: 687725.

    • Search Google Scholar
    • Export Citation
  • 2.

    Herrer A, Christensen HA, 1976. Natural cutaneous leishmaniasis among dogs in Panamá. Am J Trop Med Hyg 25: 5963.

  • 3.

    Aguilar CM, Fernandez E, Fernandez R, Deane LM, 1984. Study of an outbreak of cutaneous leishmaniasis in Venezuela: the role of domestic animals. Mem Inst Oswaldo Cruz 79: 181195.

    • Search Google Scholar
    • Export Citation
  • 4.

    Falqueto A, Coura JR, Barros GC, Grimaldi FG, Sessa PA, Carias VR, Jesus AC, Alencar JT, 1986. Participação do cão no ciclo de transmissão da leishmaniose tegumentar no município de Viana, Estado do Espírito Santo, Brasil. Mem Inst Oswaldo Cruz 81: 155163.

    • Search Google Scholar
    • Export Citation
  • 5.

    Herrer A, 1951. Estudio sobre leishmaniasis tegumentaria en el Peru. V. Leishmaniasis natural em perros procedentes de localidades utógenas. Rev Med Exp 8: 87117.

    • Search Google Scholar
    • Export Citation
  • 6.

    Mazza S, 1927. Leishmaniose cutánea en el caballo y nueva observacion de la misma en el perro. Bol Inst Clin Quir 3: 462464.

  • 7.

    Barros GC, Sessa PA, Mattos EA, Carias VR, Mayrink W, Alencar JT, Falqueto A, Jesus AC, 1985. Foco de leishmaniose tegumentar americana nos municípios de Viana e Cariacica, Estado do Espírito Santo, Brasil. Rev Saude Publica 19: 146153.

    • Search Google Scholar
    • Export Citation
  • 8.

    Lima WS, Dias M, Costa CA, Nogueira RH, Michalick MS, Falqueto A, 1986. Histopatologia e terapêutica da leishmaniose tegumentar canina, naturalmente adquirida. Rev Bras Med Vet Zootec 38: 3341.

    • Search Google Scholar
    • Export Citation
  • 9.

    Aguilar CM, Rangel EF, Garcia L, Fernandez E, Momen H, Grimaldi FG, Vargas Z, 1989. Zoonotic cutaneous leishmaniasis due to Leishmania (Viannia) braziliensis associated with domestic animals in Venezuela and Brazil. Mem Inst Oswaldo Cruz 84: 1928.

    • Search Google Scholar
    • Export Citation
  • 10.

    Falqueto A, Sessa PA, Varejão JB, Barros GC, Momem H, Grimaldi G Jr, 1991. Leishmaniasis due to Leishmania braziliensis in Espirito Santo state: further evidence on the role of dogs as a reservoir of infection for humans. Mem Inst Oswaldo Cruz 86: 499500.

    • Search Google Scholar
    • Export Citation
  • 11.

    Cunha JC, Lima JW, Pompeu MM, 2006. Transmissão domiciliar de leishmaniose tegumentar e associação entre leishmaniose humana e canina, durante uma epidemia na Serra do Baturité, no estado do Ceará, Brasil. Rev Bras Epidemiol 9: 425435.

    • Search Google Scholar
    • Export Citation
  • 12.

    Oliveira-Neto MP, Pirmez C, Rangel E, Schubach A, Grimaldi G Jr, 1988. An outbreak of american cutaneous leishmaniasis (Leishmania braziliensis braziliensis) in a periurban area of Rio de Janeiro city, Brazil: clinical and epidemiological studies. Mem Inst Oswaldo Cruz 83: 427435.

    • Search Google Scholar
    • Export Citation
  • 13.

    Rangel EF, Azevedo AC, Andrade CA, Souza NA, Wermelinger ED, 1990. Studies on sand fly fauna (Diptera: Psychodidae) in a foci of cutaneous leishmaniasis in Mesquita, Rio de Janeiro state, Brazil. Mem Inst Oswaldo Cruz 85: 3945.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ferreira AL, Sessa PA, Varejão JB, Falqueto A, 2001. Distribution of sand flies (Diptera: Psychodidae) at different altitudes in an endemic region of american cutaneous leishmaniasis in the State of Espírito Santo, Brazil. Mem Inst Oswaldo Cruz 96: 10611067.

    • Search Google Scholar
    • Export Citation
  • 15.

    Alexander B, de Oliveria EB, Haigh E, de Almeida LL, 2002. Cutaneous leishmaniasis in coffee plantations of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 97: 627630.

    • Search Google Scholar
    • Export Citation
  • 16.

    Coutinho JO, Barreto MP, 1941. Dados bionômicos sobre o Phlebotomus fischeri Pinto, 1926 (Diptera, Psychodidae). Rev Bras Biol 1: 423429.

    • Search Google Scholar
    • Export Citation
  • 17.

    Alencar RB, 2007. Emergência de flebotomíneos (Diptera: Psychodidae) em chão de floresta de terra firme na Amazônia Central do Brasil: Uso de um modelo modificado de armadilha de emergência. Acta Amazon 37: 287292.

    • Search Google Scholar
    • Export Citation
  • 18.

    Arias JR, Freitas RA, 1982. On the vectors of cutaneous leishmaniasis in the Central Amazon of Brazil. 4. Sand fly emergence from a “terra firme” forest floor. Acta Amazon 12: 609611.

    • Search Google Scholar
    • Export Citation
  • 19.

    Bettini S, Contini C, Atzeni MC, Tocco G, 1986. Leishmaniasis in Sardinia. I. Observations on a larval breeding site of Phlebotomus perniciosus, Phlebotomus perfiliewi perfiliewi and Sergentomyia minuta (Diptera: Psychodidae) in the canine leishmaniasis focus of Soleminis (Cagliari). Ann Trop Med Parasitol 80: 307315.

    • Search Google Scholar
    • Export Citation
  • 20.

    Doha S, Kamal H, Shehata M, Helmy N, Kader MA, El Said S, El Sawaf BM, 1990. The breeding habitats of Phlebotomus sand flies (Diptera: Psychodidae) in Al Agamy, Alexandria, Egypt. J Egypt Soc Parasitol 20: 747752.

    • Search Google Scholar
    • Export Citation
  • 21.

    Feliciangeli MD, 2004. Natural breeding places of phebotomine sandflies. Med Vet Entomol 18: 7180.

  • 22.

    Pifano CF, 1941. La leishmaniosis tegumentaria en el estado Yaracuy, Venezuela. Gac Med Caracas 48: 292299.

  • 23.

    Forattini OP, 1954. Algumas observações sobre biologia de flebótomos (Diptera, Psychodidae) em região da bacia do rio Paraná (Brasil). Arq Fac Hig Saúde Públ 8: 15136.

    • Search Google Scholar
    • Export Citation
  • 24.

    Forattini OP, 1960. Novas observações sobre a biologia de flebótomos em condições naturais (Diptera, Psychodidae). Arq Fac Hig Saúde Públ 25: 209215.

    • Search Google Scholar
    • Export Citation
  • 25.

    Ferro C, Pardo R, Torres M, Morrison A, 1997. Larval microhabitats of Lutzomyia longipalpis (Diptera: Psychodidae) in a endemic focus of visceral leishmaniasis in Colombia. J Med Entomol 34: 719728.

    • Search Google Scholar
    • Export Citation
  • 26.

    Casanova C, 2001. A soil emergence trap for collections of phlebotomine sand flies. Mem Inst Oswaldo Cruz 96: 273275.

  • 27.

    Deane LM, Deane MP, 1957. Observações sobre abrigos e criadouros de flebótomos no noroeste do Estado do Ceará. Rev Bras Malariol Doencas Trop 9: 225246.

    • Search Google Scholar
    • Export Citation
  • 28.

    Oliveira CD, Assunção RM, Reis IA, Proietti FA, 2001. Spatial distribution of human and canine visceral leishmaniasis in Belo Horizonte, Minas Gerais State, Brasil, 1994–1997. Cad Saude Publica 17: 12311239.

    • Search Google Scholar
    • Export Citation
  • 29.

    Costa CH, Tapety CM, Werneck GL, 2007. Controle da leishmaniose visceral em meio urbano: estudo de intervenção randomizado fatorial. Rev Soc Bras Med Trop 40: 415419.

    • Search Google Scholar
    • Export Citation
  • 30.

    Werneck GL, 2008. Forum: geographic spread and urbanization of visceral leishmaniasis in Brazil. Introduction. Cad Saude Publica 24: 29372940.

    • Search Google Scholar
    • Export Citation
  • 31.

    Costa CH, Pereira HF, Araújo MV, 1990. Epidemia de leishmaniose visceral no estado do Piauí, Brasil, 1980–1986*. Rev Saude Publica 24: 361372.

    • Search Google Scholar
    • Export Citation
  • 32.

    Disney RH, 1966. A trap for phlebotomine sandflies attracted to rats. Bull Entomol Res 56: 445451.

  • 33.

    Peel MC, Finlayson BL, McMahon TA, 2007. Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11: 16331644.

  • 34.

    Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A, 2005. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25: 19651978.

    • Search Google Scholar
    • Export Citation
  • 35.

    Shannon R, 1939. Methods for colleting and feeding mosquitoes in jungle yellow fever studies. Am J Trop Med Hyg 19: 131140.

  • 36.

    Young DG, Duncan MA, 1994. Guide to the Identification and Geographic Distribuition of Lutzomyia Sand Flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae). Gainesville, FL: Associated Publishers of the American Entomological Institute.

    • Search Google Scholar
    • Export Citation
  • 37.

    Camargo-Neves VL, Gomes AC, Antunes JL, 2002. Correlação da presença de espécies de flebotomíneos (Diptera: Psychodidae) com registros de casos da leishmaniose tegumentar americana no Estado de São Paulo, Brasil. Rev Soc Bras Med Trop 35: 299306.

    • Search Google Scholar
    • Export Citation
  • 38.

    Rangel EF, Souza NA, Wermelinger ED, Barbosa AF, 1984. Infecção natural de Lutzomyia intermedia Lutz & Neiva 1912, em área endêmica de leishmaniose tegumentar no Estado do Rio de Janeiro. Mem Inst Oswaldo Cruz 79: 395396.

    • Search Google Scholar
    • Export Citation
  • 39.

    Azevedo AC, Rangel EF, Queiroz RG, 1990. Lutzomyia migonei (França, 1920) naturally infected with peripylarian flagellates in Baturité, a focus of cutaneous leishmaniasis in Ceará State, Brazil. Mem Inst Oswaldo Cruz 85: 479.

    • Search Google Scholar
    • Export Citation
  • 40.

    Falqueto A, Varejão JB, Sessa PA, 1987. Cutaneous leishmaniasis in a horse (Equus caballus) from endemic area in the state of Espírito Santo, Brazil. Mem Inst Oswaldo Cruz 82: 443.

    • Search Google Scholar
    • Export Citation
  • 41.

    Dougherty MJ, Guerin PM, Ward RD, 1994. Isolation of oviposition pheromone from the eggs of the sandfly Lutzomyia longipalpis. Med Vet Entomol 8: 119124.

    • Search Google Scholar
    • Export Citation
  • 42.

    Dougherty MJ, Guerin PM, Ward RD, 1995. Identification of oviposition attractants for the sandfly Lutzomyia longipalpis (Diptera: Psychodidae) in volatiles of feces from vertebrates. Physiol Entomol 20: 2332.

    • Search Google Scholar
    • Export Citation
  • 43.

    Pita-Pereira D, Souza GD, Pereira TA, Zwetsch A, Britto C, Rangel EF, 2011. Lutzomyia (Pintomyia) fischeri (Diptera: Psychodidae: Phlebotominae), a probable vector of American cutaneous leishmaniasis: detection of natural infection by Leishmania (Viannia) DNA in specimens from the municipality of Porto Alegre (RS), Brazil, using multiplex PCR assay. Acta Trop 120: 273275.

    • Search Google Scholar
    • Export Citation
  • 44.

    Rocha LS, Falqueto A, Santos CB, Ferreira AL, Graça GC, Grimaldi G Jr, Cupolillo E, 2010. Survey of natural infection by Leishmania in sand fly species collected in southeastern Brazil. Trans R Soc Trop Med Hyg 104: 461466.

    • Search Google Scholar
    • Export Citation
  • 45.

    Alexander B, Maroli M, 2003. Control of phlebotomine sandflies. Med Vet Entomol 17: 118.

  • 46.

    Falcão AL, Falcão AR, Pinto CT, Contijo CM, Falqueto A, 1991. Effect of deltamethrin spraying on the sandfly populations in a focus of american cutaneous leishmaniasis. Mem Inst Oswaldo Cruz 86: 399404.

    • Search Google Scholar
    • Export Citation
  • 47.

    Teodoro U, Thomaz-Soccol V, Kühl JB, Santos DR, Santos ES, Santos AR, Abbas M, Dias AC, 2004. Reorganization and cleanness of peridomiciliar area to control sand flies (Diptera, Psychodidae, Phlebotominae) in South Brazil. Braz Arch Biol Technol 47: 205212.

    • Search Google Scholar
    • Export Citation
  • 48.

    Teodoro U, Santos DR, Santos AR, Oliveira O, Santos ES, Neitzke HC, Monteiro WM, Rossi RM, Lonardoni MV, Silveira TG, 2006. Avaliação de medidas de controle de flebotomíneos no Município de Lobato, Estado do Paraná, Sul do Brasil. Cad Saude Publica 22: 451455.

    • Search Google Scholar
    • Export Citation
  • 49.

    Reinhold-Castro KR, Scodro RB, Dias-Sversutti AC, Neitzke HC, Rossi RM, Kühl JB, Silveira TGV, Teodoro U, 2008. Avaliação de medidas de controle de flebotomíneos. Rev Soc Bras Med Trop 41: 269276.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Aloísio Falqueto, Unidade de Medicina Tropical, Universidade Federal do Espírito Santo, Av Marechal Campos 1468, 29043-900 Vitória, ES, Brazil. E-mail: falqueto@npd.ufes.br

Authors' addresses: Vivaldo Pim Vieira, Adelson Luiz Ferreira, Claudiney Biral dos Santos, Gustavo Rocha Leite, Gabriel Eduardo Melim Ferreira, and Aloísio Falqueto, Universidade Federal do Espírito Santo, Unidade de Medicina Tropical Vitória, Espírito Santo, Brazil, E-mails: vivapim@hotmail.com, claudineybiral@gmail.com, gugarl@gmail.com, adelsonlf@hotmail.com, gmelim@ioc.fiocruz.br, and falqueto@npd.ufes.br.

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