Twenty-eight years of Aedes albopictus in Brazil : a rationale to maintain active entomological and epidemiological surveillance

Introduction: Aedes albopictus was fi rst detected in Brazil in 1986. This mosquito species presents a major threat to public health because Brazilian populations have shown substantial vector competence for arboviruses such as dengue and chikungunya. Methods: We updated the records of Ae. albopictus in several States of Brazil, focusing on areas in which its presence had been reported after 2002. Results: Twenty-eight years after its arrival in Brazil, Ae. albopictus has been detected in 24 of 27 States. Conclusions: The rapid spread of this species and its high vector competence demonstrate the danger of Ae. albopictus in Brazil.

Aedes albopictus (Skuse 1894) originated in Southeast Asia, where it is implicated in the transmission of the dengue virus in several countries (1) .The spread of Ae. albopictus to Europe, Africa, and the Americas has raised major public health concerns as this species is not only an important vector for the dengue virus, but may also transmit other arboviral infections, such as yellow fever, chikungunya, and several encephalitides (2) .Aedes albopictus has a broad distribution in tropical as well as temperate countries (1) , even more so than Aedes aegypti (Linnaeus 1762).
In Brazil, Ae. albopictus has not yet been incriminated as a dengue vector, although it has been shown, under artifi cial conditions, that Brazilian populations of this species are capable of being infected with the dengue virus, and successfully transmitting it (3) .Recently, under laboratory conditions, Brazilian populations of Ae. albopictus have also shown high vector competence for the chikungunya virus, reinforcing the importance of entomological and epidemiological surveillance of this mosquito species in Brazil (4) .
Aedes albopictus was fi rst recorded in Brazil in 1986.It occurred in the southeast of Brazil, in the State of Rio de Janeiro, with 6 females and 5 males of this species confi rmed from specimens collected at Rodovia Rio-São Paulo, Km 47 (5) .In the same year, 3 larvae of Ae. albopictus were identifi ed in the State of São Paulo, in the Areias municipality (6) .Within a few years, Ae. albopictus had been recorded in all four southeastern States of Brazil (1) .
The fi rst record of Ae. albopictus in southern Brazil occurred in the State of Paraná in 1996 (7) .Females of this mosquito species were captured in the City of Curitiba using human bait (7) .
In December 1997, during the routine activities of the Brazilian Dengue Control Program in Mato Grosso do Sul in west-central Brazil, fourth stage larvae (n = 3) and pupae (n = 5) of Ae. albopictus were collected from a tree hole in the municipality of Douradina (8) .
In April 2002, employees of the Brazilian Dengue Control Program detected Ae. albopictus larvae in larvitraps in the municipality of Medicilândia, Pará, in northern Brazil.This was the fi rst record of Ae. albopictus in the State of Pará.One month later, 42 adult (23 males and 19 females) Ae. albopictus were captured with human bait during the morning hours (9) .
The distribution of Ae. albopictus in Brazil was described in 2003, where 7 of its 27 states had not registered the presence of this mosquito species: Acre, Amapá, Ceará, Piauí, Roraima, Sergipe, and Tocantins (10) .Slightly more than 10 years later, this situation has changed: Ae. albopictus has now also been detected in Ceará, Tocantins, Roraima, and Piauí (Figure 1 and Table 1).
Between January and July 2005, the Brazilian Dengue Control Program of the State of Ceará, in northeastern Brazil, collected Aedes eggs during routine field activities.After eclosion, the immature mosquitoes were raised in the laboratory to the adult stage.In one neighborhood of the City of Fortaleza, Montese, 13 Ae.albopictus adults were reared from eggs collected in domestic and peridomestic areas -the fi rst report of this species in Ceará (11) .It is important to note that in the

ACKNOWLEDGMENTS
The authors declare that there is no confl ict of interest.

State Year Stage of life cycle
Rio de Janeiro (5) 1986 adult São Paulo (6) 1986 larvae Paraná (7) 1996 adult Mato Grosso do Sul (8) 1997 larvae and pupae Pará (9) 2002 larvae and adult Ceará (11) 2005 eggs Tocantins (13) 2006 larvae and pupae Roraima (14) 2006 larvae and pupae same city, serotypes DENV-2 and DENV-3 were recently isolated from pools containing Ae. albopictus females deprived of having a blood meal; this demonstrates the occurrence of vertical transmission of the dengue virus among this population (12) .Aedes albopictus was found for the fi rst time in the State of Tocantins, in northern Brazil, between January and February of 2006, during entomological surveillance for Ae.aegypti in the municipality of Mateiros.One larva and three Ae.albopictus pupae were identifi ed (13) .
In June 2006, Ae. albopictus was found for the fi rst time in the State of Roraima, in the capital Boa Vista, where two pupae of Ae. albopictus were collected during the Brazilian Dengue Control Program.In November of the same year, another pupa was collected, and in May 2007, 10 larvae of this species were collected in 3 neighborhoods of Boa Vista: Araceli Souto Maior, Cinturão Verde, and Pricumã (14) .
Aedes albopictus was detected in the State of Piauí during annual larval surveys conducted during 2007-2014.Data were collected using a house-to-house larval survey (Larval Index) and the "Rapid Assessment of Infestation by Aedes aegypti" (LIRAa) (15) .
The rapid geographical spread of Ae. albopictus in different continents was thought to have only minimal consequences for humans, because this mosquito species has been considered to have a relatively low capacity to transmit pathogens.Aedes albopictus is considered exophilic, exophagic, and common in rural and vegetated suburban areas in Brazil (1) .Nevertheless, it can bloodfeed on different vertebrate hosts besides humans and, owing to its opportunistic feeding behavior, may serve as a bridge vector for the transmission of emerging viruses, such as yellow fever, between wild and domestic animals and humans (10) .
The dengue and chikungunya arboviruses are commonly transmitted by the same mosquito vectors: Ae. aegypti and Ae.albopictus.The latter species rapidly spread through Brazil, such that only three States have not yet registered its presence.The rapid spread of Ae. albopictus, in conjunction with the high vector competence of Brazilian populations of this species to the dengue and chikungunya arboviruses (3) (4) confi rm its threat to the population of Brazil.
It is important to note that most records of Ae. albopictus in Brazilian states occurred during entomological surveillance, which involves the regular monitoring of existent, or potential, mosquito vectors of human disease.Therefore, it is extremely important to maintain entomological and epidemiological surveillance and/or control of Ae. albopictus in all municipalities of all Brazilian States, in order to minimize future arbovirus outbreaks.
The authors thank Dr. Phil Lounibos for the help with the English in the manuscript and Lucas Rodrigues for the map.

Pancetti
FGM et al. -Monitoring Ae. albopictus in Brazil