Lutzomyia longipalpis ( Diptera , Psychodidae , Phlebotominae ) and urbanization of visceral leishmaniasis in Brazil Lutzomyia longipalpis ( Diptera , Psychodidae , Phlebotominae )

The article discusses habits related to the vectorial competence of Lutzomyia longipalpis, along with evidence confirming the importance of this sand fly species in the epidemiological chain of visceral leishmaniasis in Brazil. A new epidemiological profile for visceral leishmaniasis is also postulated, associated with domestic environments and the role of Lu. longipalpis in this process, its sylvatic origin, and its capacity to adapt to a wide range of habitats. Another sand fly species, Lu. cruzi, is mentioned as a vector of visceral leishmaniasis in some municipalities in Central Brazil, based on studies in endemic areas of the

The history of visceral leishmaniasis in Brazil was initially associated with the rural environment, based especially on studies in Sobral, Ceará State, from 1954 to 1956, when a serious epidemic led to dozens of deaths.At the time, the logic was that dogs and the vector were links in the epidemiological chain in the domestic setting.Lutzomyia longipalpis was identified as the vector, based on consistent evidence from various studies concerning this sand fly's vectorial competence 1,2,3 .
Drastic environmental alterations caused by human action have changed the ecology of some sand fly species and leishmanias and thus the epidemiology of the leishmaniases.Therefore, a new transmission profile should be considered, in which humans are no longer accidental hosts, since they now live in close and frequent association with the epidemiological chain 4 .Continuous deforestation and slashing-and-burning on the expanding agricultural frontiers, extractivism, rural settlements, wildcat mining camps, and dams and hydroelectric plants are factors that can favor outbreaks.Steady migratory flows constitute another socioeconomic component, with poor populations in underdeveloped countries seeking to improve their quality of life by moving to urban areas 4 .
Transmission of visceral leishmaniasis has been reported in more than 1,600 municipalities in 19 of the 27 Brazilian States and is present to date in all regions of the country except perhaps the South.An epidemiological evaluation of the last 13 years shows alterations in the transmission profile, originally characterized by a rural pattern (with only occasional cases on the periphery of some cities), but with the current profile associated with large cities like Corumbá (Mato Grosso do Sul) and Araçatuba (São Paulo) and some State capitals, including Campo Grande (Mato Grosso do Sul), Belo Horizonte (Minas Gerais), Palmas (Tocantis), Teresina (Piauí), and São Luís (Maranhão) 5 .
Lu. longipalpis is the most important visceral leishmaniasis vector in the Americas, and is certainly the only sand fly species (including those associated with transmission of the etiological agents of tegumentary leishmaniasis) that meets all the established criteria for vectorial competence 6 , highlighting those that are considered essential, like anthropophilia, spatial distribution coinciding with human cases of the disease, and natural infection by Leishmania (L.) infantum chagasi 3,6,7,8 .
In Brazil, Lu. longipalpis, although already displaying extensive geographic distribution, appears to be undergoing further territorial expansion, with Acre, Amazonas, Amapá, Paraná, Santa Catarina, and Rio Grande do Sul as the only States that have still not reported cases 5 .
Pioneering reports on the sylvatic origin of Lu. longipalpis were obtained from studies conducted most consistently in the North, where the species was believed to be participating in the primary transmission chain of L. (L.) infantum chagasi.In the State of Pará, the species was shown to be sylvatic, while adapting to human dwellings in impacted areas 9,10,11 .It was suggested that the species occurred in forests, far from dwellings, but with particularly eclectic habits and great capacity to adapt to the peridomicile (chicken coops) around houses built along roads, as along the highway that connected Igarapé-Mirí to Tucuruí, were Lu.longipalpis had invaded residences after just 18 months of highway construction (there was evidence that Lu. longipalpis females were feeding on a variety of mammals and invading residences) 12 .Based on research in the Amazon Region, it was also suggested that this sand fly could establish its breeding sites in forest areas.
By 1973, reports 13 in the Southeast and Northeast of Brazil already showed the presence of Lu. longipalpis inside human dwellings and in outbuildings with domestic and farm animals, including donkey corrals.
This sand fly gradually colonized the rural environment, and in the late 1980s the species began invading the urban environment, especially the periphery of large cities, where it was captured in the intradomiciliary and peridomiciliary settings (in the latter case in outbuildings with domestic animals) 8 .
One can logically suppose that some aspects of Lu. longipalpis behavior play a determinant role in this context of urbanization of visceral leishmaniasis, especially its flexible eating habits (an eclectic search for blood meal sources) and easy adaptation to domestic conditions, allowing positive captures inside human dwellings and animal pens.
In the 1980s, outbreaks of visceral leishmaniasis in Teresina and São Luís motivated the development of epidemiological studies, including those focusing on the Lu.Longipalpis vector 14,15,16,17 .
In the State of Piauí, visceral leishmaniasis has been reported since 1934 14 .In 1980, as the disease spread, the urban area of the State capital Teresina recorded a large number of human cases 15 , subsequently confirming the concentration of the disease inside the city limits 16 .Based on observations, Lu. longipalpis was infesting human dwellings, and it was possible to hypothesize a positive correlation between the number of human cases and the household vector infestation rate 15 .In 1994, naturally infected specimens of Lu. longipalpis were captured in Teresina, thus corroborating the vector's infection in the urban setting 17 .Later (2001), Lu. longipalpis continued to be captured in human dwellings in Piauí 18 , clearly demonstrating the sand fly's adaptation to the urban setting.
The outbreak of visceral leishmaniasis in São Luís, Maranhão, in 1983, led to an increase in research on the vector, showing both the anthropophilia of Lu.Longipalpis and specimens naturally infected with suprapylarian promastigotes, suggested as Leishmania 19 .Since then, in this same municipality, studies have aimed to expand the knowledge on the sand fly's habits.The species has been shown to live in perfect harmony with humans and domestic animals, and its seasonality and hourly occurrence in the intra and peridomicile have been identified.The species has been found with high density in nearly every month of the year, and has been captured throughout the night, but especially from 8:00 PM to 2:00 AM in the intradomicile and from 6:00 to 10:00 PM in the peridomicile 20,21 .According to recent studies on the island of São Luís, Lu. longipalpis adapts easily to the human environment 22,23 .
More recently, Campo Grande, capital of the Brazilian State of Mato Grosso do Sul, reported the spread of visceral leishmaniasis in the urban environment, leading to more systematic studies on Lu. longipalpis.
Mato Grosso do Sul is perhaps the State where the leishmaniases pose the worst public health problem, especially visceral leishmaniasis, which has been endemic since 1980 in some cities classified as having intense transmission, particularly Corumbá 24,25 .Based on reports of human visceral leishmaniasis in Corumbá in the 1980s, studies were done to verify the vector's presence.The most frequent sand fly species included Lu. cruzi, showing high density in the intra and peridomicile as an anthropophilic species 26 .Lu. cruzi naturally infected with L. (L.) infantum chagasi was later reported, and considering the apparent absence of Lu. longipalpis, the former sand fly was suggested as the vector for visceral leishmaniasis in the Corumbá/Ladário region 27 .While the disease was initially limited to this region, in 1995 it began spreading, and 2002 witnessed the first reports of autochthonous human cases in Campo Grande, with a gradual increase in the number of reported cases 28 .In 2000, Lu. longipalpis had already been detected in the urban area of this municipality 29 .Recently, in 2006 25 , studies on the sand fly fauna in the urban area of Campo Grande showed clearly that Lu. longipalpis was the most abundant species (92.22%) in the human environment, pointing to a six-fold increase in this sand fly's density as compared to studies from 1999-2000.Based on these data, the authors suggest that the high density of Lu. longipalpis is the principal risk factor for visceral leishmaniasis transmission in the urban area.As a whole, the studies in Campo Grande 28 showed that this sand fly is highly anthropophilic, although displaying exceptionally eclectic eating habits.
Clearly, the history of visceral leishmaniasis epidemiology in Brazil has shown a constant role for Lu.longipalpis as an essential link in the transmission chain.Its ability to feed frequently on domestic and synanthropic animals, as well as its noteworthy anthropophilia, favor Lu. longipalpis in its adaptation to modified environments, meanwhile allowing the maintenance of the visceral leishmaniasis transmission cycle in the rural environment and its spread to urbanized areas, thus leading to differentiated transmission profiles.This sand fly's gradual encroachment from the sylvatic environment into periurban areas and the observation of the evident urbanization process, the result of the vector's competence for colonizing impacted areas, highlight the importance of entomological surveillance and monitoring measures for qualitative and quantitative assessment of the vector.Importantly, there is a need to add new knowledge on Lu.Longipalpis biology, especially considering entomological indicators, like the infection rate, with a view towards surveillance measures.