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Emergence of Aedes aegypti in Madeira island: origin, insecticide resistance and vector competence
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Aedes aegypti é altamente competente para a transmissão aos humanos de arbovírus, como chikungunya, dengue e Zika. A recente expansão desta espécie para áreas de onde foi eliminada e o seu estabelecimento em novos territórios, combinada com um crescimento urbano intensivo e aumento do movimento global de pessoas e mercadorias, desencadearam o dramático aumento da incidência de arboviroses nos últimos 40 anos. A vulnerabilidade da Europa aos arbovírus está a aumentar em áreas onde as populações de mosquitos vetores estão presentes. Um exemplo notável é o recente surto de dengue na ilha da Madeira em 2012. Apesar das medidas de controlo vetorial implementadas, a espécie Ae. aegypti encontra-se em contínua expansão desde o momento da sua introdução em 2005. Neste contexto, foram analisadas populações de Ae. aegypti da ilha da Madeira com o objetivo de i) caracterizar a sua suscetibilidade aos inseticidas e os potenciais mecanismos de resistência presentes, ii) determinar a origem geográfica de Ae. aegypti da região e a sua estrutura genética com recurso a marcadores genéticos, tais como microssatélites e ADN mitocondrial, e iii) avaliar a competência da espécie presente na ilha para a transmissão dos vírus chikungunya, dengue e Zika.
A espécie Aedes aegypti presente na Madeira foi considerada resistente a todos os inseticidas testados. Ensaios efetuados com sinergistas, que aumentaram significativamente as taxas de mortalidade, juntamente com os ensaios bioquímicos, que indicaram atividades enzimáticas aumentadas, sugerem a presença de resistência metabólica. A análise de microarrays revelou o aumento da expressão de genes associados à resistência aos inseticidas, principalmente proteínas cuticulares e citocromo oxidases P450. Destes, os genes mais expressos, Cyp9J32 e Cyp9J28, são conhecidos metabolizadores de piretróides. A genotipagem de mutações kdr revelou a presença da mutação V1016I com uma frequência moderada enquanto a mutação F1534C encontra-se fixa.
As análises de genética populacional indicam pelo menos dois eventos de colonização de Ae. aegypti na Madeira, sendo a Venezuela o mais provável país de origem destas introduções. Estimativas de tamanho efetivo populacional são consistentes com a rápida expansão de Ae. aegypti na ilha, atingindo valores máximos em 2012, coincidente com o surto de dengue ocorrido neste ano. Mais ainda, os resultados sugerem que as medidas de controlo implementadas após o surto podem ter afetado o tamanho efetivo de Ae. aegypti no Funchal.
Finalmente, os estudos de competência vetorial revelaram a elevada suscetibilidade para a transmissão dos vírus chikungunya e dengue e moderada suscetibilidade para a transmissão do vírus Zika. Em conjunto, os resultados obtidos corroboram o potencial risco para a disseminação de arbovírus na população local de Ae. aegypti. Assim, é necessário que a Madeira mantenha, atualize e teste os planos de contigência para estas arboviroses, de modo a garantir a devida preparação para futuras epidemias. Mais ainda, este estudo contribuiu para uma melhor compreensão do estado de resistência aos inseticidas e da estrutura genética de populações de Ae. aegypti na ilha, conhecimentos que poderão ser usados no delineamento e implementação de novas estratégias de controlo que previnam novos surtos arbovíricos transmitido por esta espécie.
Aedes aegypti is highly competent to transmit arboviruses to humans, such as chikungunya, dengue and Zika. The recent expansion of this species into areas where it has been eliminated and its establishment in new territories, combined with intensive urban growth and increased global movement of people and goods, have triggered a dramatic increase in the incidence of arboviruses over the last 40 years. The vulnerability of Europe to arboviruses is increasing in areas where mosquito vector populations are present. A striking example is the recent dengue outbreak on Madeira Island in 2012. Despite the vector control measures implemented, Ae. aegypti has been in continuous expansion since its introduction in 2005. In this context, Ae. aegypti populations from Madeira Island were analysed with the objective of i) characterize their susceptibility to insecticides and potential resistance mechanisms present, ii) determine the geographical origin of Ae. aegypti in the region and its genetic structure using genetic markers such as microsatellites and mitochondrial DNA, and iii) evaluate the competence of the species present on the island for chikungunya, dengue and Zika viruses transmission. The Aedes aegypti of Madeira was considered resistant to all insecticides tested. Bioassays performed with synergists, which significantly increased mortality rates, along with biochemical assays, which indicated increased enzymatic activities, suggest the presence of metabolic resistance. Microarray analysis revealed increased expression of genes associated with insecticide resistance, mainly cuticle proteins and cytochrome P450 oxidases. Of these, the most expressed genes, Cyp9J32 and Cyp9J28, are known pyrethroid metabolizers. Genotyping of kdr mutations revealed the presence of the V1016I mutation at a moderate frequency while the F1534C mutation is fixed. Population genetics analyses suggest at least two colonization events of Ae. aegypti in Madeira, with Venezuela being the most likely origin of these introductions. Effective population size estimates are consistent with a rapid expansion of Ae. aegypti on the island, reaching maximum values in 2012, coinciding with the dengue outbreak in this year. Moreover, results suggest that the control measures implemented after the outbreak may have affected the Ae. aegypti effective size in Funchal. Finally, vector competence studies revealed high susceptibility for chikungunya and dengue viruses transmission and moderate susceptibility to Zika virus transmission. Altogether, the results obtained corroborate the potential risk for the dissemination of arboviruses in the local population of Ae. aegypti. Thus, it is necessary for Madeira to maintain, update and test contingency plans for these arboviruses in order to ensure proper preparation for future epidemics. Moreover, this study contributed to a better understanding of insecticide resistance status and the population genetic structure of Ae. aegypti populations on the island, knowledge that may be used in the design and implementation of new control strategies to prevent new outbreaks of arboviruses transmitted by this species.
Aedes aegypti is highly competent to transmit arboviruses to humans, such as chikungunya, dengue and Zika. The recent expansion of this species into areas where it has been eliminated and its establishment in new territories, combined with intensive urban growth and increased global movement of people and goods, have triggered a dramatic increase in the incidence of arboviruses over the last 40 years. The vulnerability of Europe to arboviruses is increasing in areas where mosquito vector populations are present. A striking example is the recent dengue outbreak on Madeira Island in 2012. Despite the vector control measures implemented, Ae. aegypti has been in continuous expansion since its introduction in 2005. In this context, Ae. aegypti populations from Madeira Island were analysed with the objective of i) characterize their susceptibility to insecticides and potential resistance mechanisms present, ii) determine the geographical origin of Ae. aegypti in the region and its genetic structure using genetic markers such as microsatellites and mitochondrial DNA, and iii) evaluate the competence of the species present on the island for chikungunya, dengue and Zika viruses transmission. The Aedes aegypti of Madeira was considered resistant to all insecticides tested. Bioassays performed with synergists, which significantly increased mortality rates, along with biochemical assays, which indicated increased enzymatic activities, suggest the presence of metabolic resistance. Microarray analysis revealed increased expression of genes associated with insecticide resistance, mainly cuticle proteins and cytochrome P450 oxidases. Of these, the most expressed genes, Cyp9J32 and Cyp9J28, are known pyrethroid metabolizers. Genotyping of kdr mutations revealed the presence of the V1016I mutation at a moderate frequency while the F1534C mutation is fixed. Population genetics analyses suggest at least two colonization events of Ae. aegypti in Madeira, with Venezuela being the most likely origin of these introductions. Effective population size estimates are consistent with a rapid expansion of Ae. aegypti on the island, reaching maximum values in 2012, coinciding with the dengue outbreak in this year. Moreover, results suggest that the control measures implemented after the outbreak may have affected the Ae. aegypti effective size in Funchal. Finally, vector competence studies revealed high susceptibility for chikungunya and dengue viruses transmission and moderate susceptibility to Zika virus transmission. Altogether, the results obtained corroborate the potential risk for the dissemination of arboviruses in the local population of Ae. aegypti. Thus, it is necessary for Madeira to maintain, update and test contingency plans for these arboviruses in order to ensure proper preparation for future epidemics. Moreover, this study contributed to a better understanding of insecticide resistance status and the population genetic structure of Ae. aegypti populations on the island, knowledge that may be used in the design and implementation of new control strategies to prevent new outbreaks of arboviruses transmitted by this species.
Descrição
Palavras-chave
Parasitologia médica Aedes aegypti Chikungunya Dengue Zika Mosquitos Vectores Resistência Ilha da Madeira
Contexto Educativo
Citação
Editora
Instituto de Higiene e Medicina Tropical