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

Abstract

INTRODUCTION:

Aedes albopictus was first 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; Update; Brazil


Aedes albopictus (Skuse 1894) originated in Southeast Asia, where it is implicated in the transmission of the dengue virus in several countries(1)Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: FIOCRUZ; 1994.. 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)Gratz NG. Critical review of the vector status of Aedes albopictus. Med Vet Entomol 2004; 18:215-227.. 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 artificial conditions, that Brazilian populations of this species are capable of being infected with the dengue virus, and successfully transmitting it(3)Castro MG, Nogueira RMR, Schatzmayr HG, Miagostovich MP,. Lourenço-de-Oliveira R Dengue virus detection by using reverse transcription-polymerase chain reaction in saliva and progeny of experimentally infected Aedes albopictus from Brazil. Mem Inst Oswaldo Cruz 2004; 99: 809-814.. 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)Vega-Rúa A, Zouache K, Girod R, Failloux AB,. Lourenço-de-Oliveira R High vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor of the spread of Chikungunya. J Virol 2014; 88:6294-6306..

Aedes albopictus was first 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 confirmed from specimens collected at Rodovia Rio-São Paulo, Km 47(5)Forattini OP. Identificação de Aedes (Stegomyia) albopictus (Skuse) no Brasil. Rev Saude Publica 1986; 20:244-245.. In the same year, 3 larvae of Ae. albopictus were identified in the State of São Paulo, in the Areias municipality(6)Brito M, Marques GRAM, Marques CCA, Tubaki RM. Primeiro encontro de Aedes (Stegomyia) albopictus (Skuse) no Estado de São Paulo (Brasil). Rev Saude Publica1986; 20:489.. Within a few years, Ae. albopictus had been recorded in all four southeastern States of Brazil(1)Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: FIOCRUZ; 1994..

The first record of Ae. albopictus in southern Brazil occurred in the State of Paraná in 1996(7)Sant'Ana AL. Primeiro encontro de Aedes (Stegomyia) albopictus (Skuse) no estado do Paraná, Brasil. Rev Saude Publica1996; 30:392-393.. Females of this mosquito species were captured in the City of Curitiba using human bait(7)Sant'Ana AL. Primeiro encontro de Aedes (Stegomyia) albopictus (Skuse) no estado do Paraná, Brasil. Rev Saude Publica1996; 30:392-393..

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)Santos SO, Nascimento JC. Primeiro registro da presença do Aedes (Stegomyia) albopictus (Skuse) em Mato Grosso do Sul, Brasil. Rev Saude Publica1998; 32:486..

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 first 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)Segura MNO, Monteiro HAO, Lopes ES, Silva OV, Castro FC, Vasconcelos PF. Encontro de Aedes albopictus no Estado do Pará, Brasil. Rev Saude Publica2003; 37:388-389..

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)10 Santos RLC. Atualização da distribuição de Aedes albopictus no Brasil (1997-2002). Rev Saude Publica2003; 37:1-4.. 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).

Figure 1:
Brazilian States that recorded Aedes albopictus during 1986-1990 (light grey: Rio de Janeiro, São Paulo, Minas Gerais, and Espírito Santo), 1991-2002 (dark grey: Amazonas, Rondônia, Pará, Goiás, Distrito Federal, Mato Grosso, Mato Grosso do Sul, Maranhão, Paraíba, Rio Grande do Norte, Pernambuco, Alagoas, Bahia, Paraná, Santa Catarina, and Rio Grande do Sul), 2003-2014 (black: Ceará, Tocantins, Roraima, and Piauí), and those with no record (white: Acre, Amapá, and Sergipe)

Table 1:
First record of Aedes albopictus in eight of Brazil's States.

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 first report of this species in Ceará(11)11 Martins VEP, Martins MG, Araújo JMP, Silva LOR, Monteiro HAO, Castro FC, et al. Primeiro registro de Aedes (Stegomyia) albopictus no Estado do Ceará, Brasil. Rev Saude Publica 2006; 40:737-739.. It is important to note that in the 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)12 Martins VE, Alencar CH, Kamimura MT, Carvalho Araújo FM, De Simone SG, Dutra RF, et al. Occurrence of natural vertical transmission of dengue-2 and dengue-3 viruses in Aedes aegypti and Aedes albopictus in Fortaleza, Ceará, Brazil. PLoS One 2012; 7:e41386..

Aedes albopictus was found for the first 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 identified(13)13 Balestra RAM, Pereira RKO, Ribeiro MJS, Silva JS, Alencar J. Ocorrência de Aedes (Stegomyia) albopictus (Skuse) em área urbana do Estado do Tocantins. Neotrop Entomol 2008; 37:233-235..

In June 2006, Aedes albopictus was found for the first 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)14 Aguiar DB, Fontão A, Rufino P, Macedo VA, Ríos-Velásquez CM, Castro MG, et al. Primeiro registro de Aedes albopictus (Diptera: Culicidae) em Roraima, Brasil. Acta Amazônica 2008; 38:357-360..

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)15 Carvalho RG, Lourenço-de-Oliveira R, Braga IA. Updating the geographical distribution and frequency of Aedes albopictus in Brazil with remarks regarding its range in the Americas. Mem Inst Oswaldo Cruz2014; 109:787-796..

The rapid geographical spread of Aedes 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)Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: FIOCRUZ; 1994.. 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)10 Santos RLC. Atualização da distribuição de Aedes albopictus no Brasil (1997-2002). Rev Saude Publica2003; 37:1-4..

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)Castro MG, Nogueira RMR, Schatzmayr HG, Miagostovich MP,. Lourenço-de-Oliveira R Dengue virus detection by using reverse transcription-polymerase chain reaction in saliva and progeny of experimentally infected Aedes albopictus from Brazil. Mem Inst Oswaldo Cruz 2004; 99: 809-814. (4)Vega-Rúa A, Zouache K, Girod R, Failloux AB,. Lourenço-de-Oliveira R High vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor of the spread of Chikungunya. J Virol 2014; 88:6294-6306. confirm its threat to the population of Brazil.

It is important to note that most records of Aedes 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.

  • 1
    Consoli RAGB, Lourenço-de-Oliveira R. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: FIOCRUZ; 1994.
  • 2
    Gratz NG. Critical review of the vector status of Aedes albopictus. Med Vet Entomol 2004; 18:215-227.
  • 3
    Castro MG, Nogueira RMR, Schatzmayr HG, Miagostovich MP,. Lourenço-de-Oliveira R Dengue virus detection by using reverse transcription-polymerase chain reaction in saliva and progeny of experimentally infected Aedes albopictus from Brazil. Mem Inst Oswaldo Cruz 2004; 99: 809-814.
  • 4
    Vega-Rúa A, Zouache K, Girod R, Failloux AB,. Lourenço-de-Oliveira R High vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor of the spread of Chikungunya. J Virol 2014; 88:6294-6306.
  • 5
    Forattini OP. Identificação de Aedes (Stegomyia) albopictus (Skuse) no Brasil. Rev Saude Publica 1986; 20:244-245.
  • 6
    Brito M, Marques GRAM, Marques CCA, Tubaki RM. Primeiro encontro de Aedes (Stegomyia) albopictus (Skuse) no Estado de São Paulo (Brasil). Rev Saude Publica1986; 20:489.
  • 7
    Sant'Ana AL. Primeiro encontro de Aedes (Stegomyia) albopictus (Skuse) no estado do Paraná, Brasil. Rev Saude Publica1996; 30:392-393.
  • 8
    Santos SO, Nascimento JC. Primeiro registro da presença do Aedes (Stegomyia) albopictus (Skuse) em Mato Grosso do Sul, Brasil. Rev Saude Publica1998; 32:486.
  • 9
    Segura MNO, Monteiro HAO, Lopes ES, Silva OV, Castro FC, Vasconcelos PF. Encontro de Aedes albopictus no Estado do Pará, Brasil. Rev Saude Publica2003; 37:388-389.
  • 10
    Santos RLC. Atualização da distribuição de Aedes albopictus no Brasil (1997-2002). Rev Saude Publica2003; 37:1-4.
  • 11
    Martins VEP, Martins MG, Araújo JMP, Silva LOR, Monteiro HAO, Castro FC, et al. Primeiro registro de Aedes (Stegomyia) albopictus no Estado do Ceará, Brasil. Rev Saude Publica 2006; 40:737-739.
  • 12
    Martins VE, Alencar CH, Kamimura MT, Carvalho Araújo FM, De Simone SG, Dutra RF, et al. Occurrence of natural vertical transmission of dengue-2 and dengue-3 viruses in Aedes aegypti and Aedes albopictus in Fortaleza, Ceará, Brazil. PLoS One 2012; 7:e41386.
  • 13
    Balestra RAM, Pereira RKO, Ribeiro MJS, Silva JS, Alencar J. Ocorrência de Aedes (Stegomyia) albopictus (Skuse) em área urbana do Estado do Tocantins. Neotrop Entomol 2008; 37:233-235.
  • 14
    Aguiar DB, Fontão A, Rufino P, Macedo VA, Ríos-Velásquez CM, Castro MG, et al. Primeiro registro de Aedes albopictus (Diptera: Culicidae) em Roraima, Brasil. Acta Amazônica 2008; 38:357-360.
  • 15
    Carvalho RG, Lourenço-de-Oliveira R, Braga IA. Updating the geographical distribution and frequency of Aedes albopictus in Brazil with remarks regarding its range in the Americas. Mem Inst Oswaldo Cruz2014; 109:787-796.
  • Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP number 2014/05016-5)

Publication Dates

  • Publication in this collection
    Feb 2015

History

  • Received
    04 July 2014
  • Accepted
    11 Nov 2014
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