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Revista Pan-Amazônica de Saúde

versão On-line ISSN 2176-6223

Rev Pan-Amaz Saude v.1 n.1 Ananindeua mar. 2010 



Phlebotominae fauna in Serra dos Carajás, Pará State, Brazil, and its possible implications for the transmission of American tegumentar leishmaniasis



Adelson Alcimar Almeida de SouzaI; Fernando Tobias SilveiraII; Ralph LainsonI; Iorlando da Rocha BarataI; Maria das Graças Soares SilvaI; José Aprígio Nunes LimaI; Maria Sueli Barros PinheiroI; Fábio Márcio Medeiros da SilvaI; Lindomar de Souza VasconcelosI; Marliane Batista CamposI; Edna Aoba Yassui IshikawaIII

IInstituto Evandro Chagas/SVS/MS, Ananindeua, Pará, Brasil
IIInstituto Evandro Chagas/SVS/MS, Ananindeua, Pará, Brasil. Núcleo de Medicina Tropical, Universidade Federal do Pará, Belém, Pará, Brasil
IIINúcleo de Medicina Tropical, Universidade Federal do Pará, Belém, Pará, Brasil

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Original Title: Fauna flebotomínica da Serra dos Carajás, Estado do Pará, Brasil, e sua possível implicação na transmissão da leishmaniose tegumentar americana. Translated by: American Journal Experts




Serra dos Carajás, located in the southeast of Pará State, Brazil, is a rich tropical forest where species of Leishmania sp. of medical interest are found, such as Leishmania (V.) braziliensis, L. (V.) lainsoni, L. (V.) shawi and L. (L.) amazonensis. They are transmitted by the following phlebotomi: Psychodopygus complexus or Ps. wellcomei, Lutzomyia ubiquitalis, Lu. whitmani and Lu. flaviscutellata. Considering the increase of immigrants in the region of the Carajás project, this study aimed to assess the Phlebotominae fauna and their possible participation in the transmission of American cutaneous leishmaniasis (ACL). The phlebotomi were captured from December 2005 to September 2007 at the following locations: i) Parauapebas Botanical Park; ii) an environmental protection area; and iii) Tapirapé-Aquiri National Forest. During the 172 days of collection, 10 CDC (18 h to 6 h) and 2 Shannon (18 h to 20 h) light traps were used. Of the 22,095 phlebotomi captured, 6,789 (31%) were male and 15,306 (69%) were female, and they belonged to 69 species and three genera, including Psychodopygus, Lutzomyia and Brumptomyia. A total of 19 (0.16%) natural infections of the following species were detected: Ps. davisi (4), Ps. h. hirsutus (3), Lu. umbratilis (3), Lu. richardward (2), Lu. brachipyga (2), Lu. ubiquitalis (2), Lu. trinidadensis (1) and Lu. migonei (1). Although no infection was found in Ps. wellcomei/complexus, the main vector of L. (V.) braziliensis in the region, this species was the most prevalent (16%), followed by Ps. davisi (15.4%), Ps. carrerai (4.2%), Lu. shawi (3.9%), Lu. brachipyga (2.5%) and Lu. richardward (1.2%). These results show the importance of these phlebotomi as possible vectors of ACL in Serra dos Carajás.

Keywords: Phlebotominae; Serra dos Carajás; Pará State; Brasil; Leishmaniasis, Cutaneous.




American cutaneous leishmaniasis (ACL) is an important public health problem in Brazil, not only due to its incidence and geographic distribution but also due to the risk of severe clinical forms of the disease. The disease is caused by different protozoan species of the genus Leishmania Ross, 1903, of which at least seven species are now recognized as being medically important in the Brazilian Amazon15,17,2. The transmission of these parasites among their primary reservoirs and, incidentally, to humans, occurs when species of the sand fly vectors feed on blood of living hosts (Diptera: Psychodidae: Phlebotominae)8,7. The genus is most diverse in the Amazon, where all the regional species that infect humans are enzootic in wild mammals belonging to several orders9,4. Humans contract the zoonotic disease when they come into contact with the sylvatic transmission cycle through hunting, swimming, panning, camping or clearing forests. The sand fly fauna of a given forested area is influenced by some variables, among which rainfall and the relative quality of food may serve to attract animal reservoirs. In Serra dos Carajás, Pará, Brazil, this fact can be observed in the region's main seasons, winter (the rainy season from December to June) and summer (the warm period from July to November), and success in capturing sand flies is greater in the rainy season than in the warm period. For this reason, it is important to study the seasonality of sand flies thought to be involved in the transmission of infection to humans14.

Our interest in researching the sand fly fauna in Serra dos Carajás dates back to the 1970s, when dozens of cases of ACL occurred among the labor force that worked on the large iron mining project, thus prompting the first investigations on the eco-epidemiology of the disease. Briefly, the main findings of this research include the description of Psychodopygus wellcomei Fraiha, Shaw and Lainson 1971, a highly anthropophilic sand fly species that incessantly bites humans in the deep forest, and its involvement as the main vector of ACL caused by Leishmania (Viannia) braziliensis in Serra dos Carajás and in other areas of the Brazilian Amazon5,12. Furthermore, we also note that altitude makes a major difference in the habitats of the potential transmitter species, Psychodopigus complexus and Ps. wellcomei: the former proliferates up to 300 m at the base of Serra18 and the latter from 300 m up to 600-700 m11.

Recently, considering the increase in immigrants in the villages surrounding the area included in the mining project in Serra dos Carajás, as well as the opening of forested areas for the establishment of new fronts for mineral exploration, a new study was established to evaluate the phlebotomine fauna in the area and its possible role in the transmission of agents of ACL. The results of this study are the subject of this report.




This study is a subproject of a research agreement between the Companhia Vale do Rio Doce (CVRD) and the Instituto   Evandro   Chagas   (IEC/SVS/MS)   entitled: "Avaliação da situação saúde-doença nas áreas de influência do Projeto Salobo e Parque Zoobotânico de Carajás, Pará, Brasil, decorrente do ecossistema local e dos movimentos migratórios - Evaluation of the health and disease situation due to the local ecosystem and migratory movements in areas influenced by the Salobo Project and Zoo and Botanical Park of Carajás, Pará, Brazil", in which we evaluated, from December 2005 to September 2007, the sand fly fauna and its possible implication in the transmission of agents of ACL.


Serra de Carajás (5° 35' - 6° 00' S and 50° 24' - 51° 06' W) is located in the southeastern region of the state of Pará, Brazil (Figure 1) and has a mixed topography of mountains and valleys, with varied vegetation consisting of primary forest and cerrado, as well as soil and subsoil rich in iron and other minerals. The average temperature in this region ranges from 20° C to 26° C with 90% relative humidity in the winter and from 26° C to 32° C with 80% humidity in the summer. Within the Serra dos Carajás, we collected sand flies from three different areas:



1- Zoo and Botanical Park Quarantine: located in the Serra dos Carajás urban center and characterized by having a small forest reserve, which borders the zoo, where it is still possible to capture sand fly vectors and wild mammals;

2- Environmental Protection Area (EPA): an area that is totally degraded by many settlements, deforestation and the housing of two heavily populated communities, Vila Sansão and Paulo Fonteles;

3- Tapirapé-Aquiri National Forest: the only primary forest reserve in which we worked. It will also be partially deforested due to a mine with copper deposits. This area is located near the Salobo camp and the Itacaiúnas River.


Two types of light traps were used to collect sand flies: the "CDC" and Shannon types. A total of 10 "CDC" type traps were used, 8 at ground level (1 m high) and 2 in the tree canopy (about 15 m to 20 m above the ground), from 18 h to 6 h, for a total collection time of 12 hours (Figure 2). Two Shannon type traps were used from 18 h to 20 h (Figure 3). These two sampling methods differ in that the "CDC" type trap catches all kinds of insects that are attracted to light, while the Shannon trap, although most insects are still attracted to the light, captures only sand flies by using a handheld suction apparatus.






The dissection of female sand flies was performed to observe the flagellates present in the intestinal tract of the insects, according to the techniques described by Ryan et al12. The females were then identified by the presence of spermathecae, and the males were mounted on slides for identification according to Young and Duncan21.


For the laboratory isolation of flagellates found in the intestinal tract of the female sand fly, mainly flagellates from the genus Leishmania, the infectious content was inoculated into Difco B4519 culture medium and intradermally into hamsters (Mesocricetus auratus). Then, after the final isolation of the parasite from culture medium, they were identified using a Leishmania-specific monoclonal antibody analysis13.



During the seven field trips to Serra dos Carajás, in three target areas (Zoo and Botanical Park Quarantine, Environmental Protection Area and Tapirapé-Aquiri National Forest), 22,095 sand fly specimens were captured: 15,306 females (69%) (Table 1) and 6,789 males (31%) (Table 2). From this total, we identified 69 different species belonging to three genera: Psychodopygus, Lutzomyia and Brumptomyia. The periods with the highest density of flies occurred between March and June, with 3,372 and 3,878 catches, respectively. On the other hand, in September, there was less activity, with only 660 specimens captured in 2006. Of all the females captured (15,306), 11,259 (73.5%) were dissected and examined for Leishmania flagellates, and 19 (0.16%) natural infections were detected in the following species of sand fly: Ps. davisi (4), Ps. h. hirsutus (3), Lutzomyia umbratilis (3), Lu. richardward (2), Lu. brachipyga (2), Lu. ubiquitalis (2), Lu. trinidadenses (1) and Lu. migonei (1) (Table 3). From the 19 natural infections detected in sand flies, eight isolates of flagellates were obtained in the Difco B4519 culture medium. The analysis using the monoclonal antibody technique13 revealed the presence of L. (V.) braziliensis in two specimens of Ps. davisi. We were unable to identify the flagellates isolated from Ps. h. hirsutus, Lu. brachipyga, Lu. richardwardi, Lu. umbratilis and Lu. ubiquitalis (Table 4). From those sand flies that were not dissected, 2,912 females were placed in the cryobank (N2 and -70° C) at IEC's Leishmaniasis Laboratory for future analysis of natural Leishmania infection by molecular methods, and 1,135 were placed in alcohol (70%) for mounting and subsequent identification.









Although we did not find a natural infection in Ps. wellcomei/complexus, the main vector for L. (V.) braziliensis in the Brazilian Amazon, this species was the most prevalent (16%) among the sand flies captured, followed by Ps. davisi (15.4%), Ps. carrerai (4.2%), Lu. shawi (3.9%), Lu. brachipyga (2.5%) and Lu. richardward (1.2%).



When discussing the sand fly fauna from Serra dos Carajás, Pará, Brazil, we should not fail to mention that previous studies have already described part of the local fauna, identifying known species and even new species of sand flies in addition to their feeding habits in relation to human and animal reservoirs20. From these findings, a description of the species Psychodopygus wellcomei Fraiha, Shaw and Lainson 1971, a highly anthropophilic sand fly that incessantly bites humans in the deep forest, and its subsequent involvement as the main vector of ACL caused by L. (V.) braziliensis in Serra dos Carajás5 was, without doubt, one of the most important discoveries related to the eco-epidemiology of ACL in Serra dos Carajás. For this reason, several attempts to colonize the sand fly in the laboratory were made to study the experimental transmission of L. (V.) braziliensis via Ps. wellcomei. Unfortunately, due to technical reasons, such as proper nutrition and the management of conditions for these sand flies, these experiments were unsuccessful. However, since one of the priorities of this study in Serra dos Carajás was to identify the vector of L. (V.) braziliensis, the principal agent of ACL in the region, large numbers of female sand flies were dissected and examined for the presence of parasite promastigotes, which resulted in the discovery of natural infections not only in Ps. wellcomei, but also in Ps. paraensis and Ps. amazonensis5. Later, it was confirmed that Ps. paraensis participates in the transmission of L. (V.) naiffi, a species not commonly found in humans6,16. Aside from those species, another species of Leishmania pathogenic to humans, L. (L.) amazonensis, has also been the subject of study in Serra dos Carajás, even though human infections are relatively rare because its vector, the sand fly Lutzomyia flaviscutellata, is not very anthropophilic8.

As with previous studies, the results of this study confirm the epidemiological importance of some species of sand flies found in the fauna of Serra dos Carajás: Ps. wellcomei and Ps. complexus, the vectors for L. (V.) braziliensis5,18, Ps. davisi, found infected with L. (V.) braziliensis, Lu. umbratilis, the vector for L. (V.) guyanensis3, Lu. ubiquitalis, the vector for L. (V.) lainsoniu16. Our results also demonstrate the great diversity of local species, with a total of 69 identified belonging to three genera: Psychodopygus, Lutzomyia and Brumptomyia. Thus, there seems to be no doubt as to the importance of Serra dos Carajás as one of the largest global areas of primitive species of sand flies.

The results of this work appear to be significant when considering the epidemiological role of some species of sand flies in transmitting ACL. This study found 19 (0.16%) natural infections in the following species of sand flies: Ps. davisi (4), Ps. h. hirsutus (3), Lu. umbratilis (3), Lu. richardward (2), Lu. brachipyga (2), Lu. ubiquitalis (2), Lu. trinidadenses (1) and Lu. migonei (1). Of all those findings, the most noticeable was, without a doubt, the discovery of four specimens of Ps. davisi with flagellates in their intestinal tracts. We were able to confirm, through identification with monoclonal antibodies, that two of these examples were naturally infected by L. (V.) braziliensis. This evidence, combined with the other discoveries of Ps. davisi naturally infected by Leishmania spp. in other locations where ACL occurs, such as Paragominas (Pará), Monte Dourado (Pará) and Serra do Navio (Amapá), substantiates our suspicion that this type of sand fly may also be involved in transmitting ACL caused by L. (V.) braziliensis in the Brazilian Amazon. Although we were not able to isolate and identify parasites in other species of sand flies, we should not fail to appreciate the presence of natural infections in Lu. umbratilis (3) and Lu. ubiquitalis (2), for example, because the importance of these species in the transmission of ACL caused by L. (V.) guyanensis and L. (V.) lainsoni, respectively16,3. is already recognized. Of the other four species naturally infected by flagellates, we should also point out that Ps. h. hirsutus and Lu. migonei naturally infected by Leishmania (V.) spp. were previously encountered in a region where ACL occurs in the states of Minas Gerais and Ceará10,1, respectively. This reinforces our suspicion that these sand flies may participate in transmitting ACL in Serra dos Carajás.

We were surprised, however, to find no specimens of Ps. wellcomei/complexus, the main vector of L. (V.) braziliensis in the Brazilian Amazon, naturally infected with a parasite, even though 1,409 females from this species were dissected. Nevertheless, this species was the most prevalent (16%) among the sand flies captured, followed by Ps. davisi (15.4%), Ps. carrerai (4.2%), Lu. shawi (3.9%), Lu. brachipyga (2.5%) and Lu. richardward (1.2%), which, in any case, supports its epidemiological importance in the research area.

Considering the findings discussed above, we feel confident in stating that the sand fly fauna of Serra dos Carajás is one of the most diverse in the world, with various species involved in the enzootic transmission of Leishmania spp. in wild animals, some of medical interest and others that have yet to be clarified.



The authors would like to acknowledge Companhia Vale do Rio Doce for financial support, the Secretariat for Health Surveillance/Ministry of Health and the IEC for logistical support and dr. Gilberta Bensabath for her dynamic work as coordinator, overcoming all the difficulties and coordinating all the programs involved. Without their participation, we would have hardly obtained the same results. We would also like to acknowledge our colleagues from the Programa de Leishmanioses at the IEC for their valuable technical assistance in the laboratory and in the field. We would like to acknowledge Antônio Francisco Pires Martins, Antônio Júlio Monteiro, Domingas Ribeiro Ervedosa, Edna de Freitas Leão, Geraldo Mendes dos Santos, João Alves Brandão, João Batista Palheta da Luz, Leônidas Souza Elizeu, Luciene Aranha da Silva, Lucivaldo João Conceição Ferreira, Raimundo Negrão Coelho, Raimundo Sérgio Machado, Raimundo Nonato Barbosa Pires, Roberto Carlos Feitosa Brandão and Rosely Conceição dos Santos de Jesus. We would like to acknowledge the secretary Vania do Socorro do Espírito Santo Monteiro for the excellent work in typing this manuscript.



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Adelson Alcimar Almeida de Souza
Instituto Evandro Chagas, Seção de Parasitologia
Rodovia BR316, km 7, s/no, Levilândia
CEP: 67030-000

Recebido em/Received/Recibido en: 30/6/2009
Aceito em/Accepted/Aceito en: 21/9/2009