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Virological Surveillance of Aedes aegypti Vectors Identifies All Four Dengue Serotypes in a Hyperendemic Region

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Abstract

Dengue virus (DENV) 1–4 is the etiological agent of dengue, the most important viral infection transmitted by Aedes spp mosquitoes to humans. Our goal was to identify the circulating DENV in Aedes aegypti collected in an area of Brazil where all four DENV serotypes had already been detected in humans, understand the epidemiology better, and to test the vector as a virological surveillance tool. Twenty-eight larvae pools and 174 females of Aedes aegypti were screened by reverse transcriptase quantitative polymerase chain reaction and semi-nested PCR assays. PCR products were sequenced, and phylogenetic analyses were performed. Nine larvae pools (32.1%) were positive for DENV, four (44.4%) with DENV-3, and five (55.6%) with more than one serotype. Fifteen females (8.6%) were positive for any DENV serotype. DENV-1 isolates belong to genotype V, DENV-2 to American–Asian genotype, DENV-3 to genotypes I and III, and DENV-4 to genotypes I and II. We demonstrate for the first time the co-circulation of all four DENV serotypes in larvae pools and adult Aedes aegypti in a hyperendemic area. This scenario represents a challenge for disease control and reinforces the importance of virological surveillance in the vector as a tool for predicting circulating DENV serotypes in humans.

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References

  • Andrade EHP, Figueiredo LB, Vilela APP, Rosa JCC, Oliveira JG, Zibaoui HM, Araújo VEM, Miranda DPJ, Ferreira PCP, Abrahão JS, Kroon EG (2016) Spatial-temporal co-circulation of Dengue virus 1, 2, 3, and 4 associated with coinfection cases in a hyperendemic area of Brazil: A 4-week survey. American Journal of Tropical Medicine and Hygiene 94(5):1080–1084

    Article  Google Scholar 

  • Bona ACD, Twerdochlib AL, Navarro-Silva MA (2011) Detection of Dengue virus in natural populations of mosquitoes. Boletín De Malariología y Saludambiental 51(2):107–116

    Google Scholar 

  • Cecílio SG, Silva Júnior WF, Tótola AH, Magalhães CLB, Ferreira JMS, Magalhães JC (2015) Dengue virus detection in Aedes aegypti larvae from southeastern Brazil. Journal of Vector Ecology 40(1):71–74

    Article  Google Scholar 

  • Chen CF, Shu PY, Teng HJ, Su CL, Wu JW, Wang JH, Lin TH (2010) Screening of Dengue virus in field-caught Aedes aegypti and Aedes albopictus (Diptera: Culicidae) by one-step SYBR green-based reverse transcriptase-polymerase chain reaction assay during 2004–2007 in Southern Taiwan. Vector-Borne and Zoonotic Diseases 10(10):1017–1725

    Article  Google Scholar 

  • da Costa CF, dos Passos RA, Lima JBP, Roque RA, Sampaio VS, Campolina TB, Secundino NFC, Pimenta PFP (2017) Transovarial transmission of DENV in Aedes aegypti in the Amazon basin: a local model of xenomonitoring. Parasites & Vectors 10(249):1–9

    Google Scholar 

  • Das B, Das M, Dwibedi B, Kar SK, Hazra RK (2013) Molecular investigations of Dengue virus during outbreaks in Orissa state, Eastern India from 2010 to 2011. Infection, Genetics and Evolution 16:401–410

    Article  CAS  Google Scholar 

  • Das S, Pingle MR, Muñoz-Jordán J, Rundell MS, Rondini S, Granger K, Chang GJ, Kelly E, Spier EG, Larone D, Spitzer E, Barany F, Golightly LM (2008) Detection and serotyping of Dengue virus in serum samples by multiplex reverse transcriptase PCR–ligase detection reaction assay. Journal of Clinical Microbiology 46(10):3276–3284

    Article  CAS  Google Scholar 

  • Ferreira-de-Lima VH, Lima-Camara TN (2018) Natural vertical transmission of dengue virus in Aedes aegypti and Aedes albopictus: a systematic review. Parasites & Vectors 11(77):1–8

    Google Scholar 

  • Figueiredo LB, Cecílio AB, Ferreira GP, Drumond BP, De Oliveira JG, Bonjardim CA, Ferreira PCP, Kroon EG (2008) Dengue virus 3 genotype I associated with dengue fever and dengue hemorrhagic fever, Brazil. Emerging Infectious Diseases 14(2):314–316

    Article  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59(3):307–321

    Article  CAS  Google Scholar 

  • Gutiérrez-Bugallo G, Rodriguez-Roche R, Díaz G, Vázquez AA, Alvarez M, Rodríguez M, Bisset JA, Guzman MG (2017) First record of natural vertical transmission of Dengue virus in Aedes aegypti from Cuba. Acta Tropica 16:146–148

    Article  Google Scholar 

  • Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, Hunsperger E, Kroeger A, Margolis HS, Martínez E, Nathan MB, Pelegrino JL, Simmons C, Yoksan S, Peeling RW (2010) Dengue: a continuing world threat. Nature Reviews Microbiology 8(12):7–16

    Article  Google Scholar 

  • Halstead SB (2008) Dengue virus-mosquito interactions. Annual Review of Entomology 53:273–291

    Article  CAS  Google Scholar 

  • Instituto Brasileiro de Geografia e Estatística (IBGE) (2010) Cidades [in portuguese]. https://cidades.ibge.gov.br/brasil/mg/contagem/panorama [accessed June 10, 2020].

  • Khan J, Khan I, Ali I, Iqbal A, Salman M (2017) The role of vertical transmission of Dengue virus among field-captured Aedes aegypti and Aedes albopictus mosquitoes in Peshawar, Khyber Pakhtunkhwa, Pakistan. Pakistan Journal of Zoology 49(3):1–7

    Google Scholar 

  • Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV (1992) Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase polymerase chain reaction. Journal of Clinical Microbiology 30(3):545–551

    Article  CAS  Google Scholar 

  • Lequime S, Paul RE, Lambrechts L (2016) Determinants of arbovirus vertical transmission in mosquitoes. Plos Pathogens 12(5):1–14

    Article  Google Scholar 

  • Martins VEP, Alencar CH, Kamimura MT, Araújo FMC, Simone SGde, Dutra RF, Guedes MIF. (2012) Occurrence of natural vertical transmission of Dengue-2 and Dengue-3 viruses in Aedes aegypti and Aedes albopictus in Fortaleza, Ceará, Brazil. PLoS ONE 7(7):1–9

    Article  Google Scholar 

  • Medeiros AS, Costa DMP, Branco MSD, Sousa DMC, Monteiro JD, Galvão SPM, Azevedo PRM, Fernandes JV, Jeronimo SMB, Araújo JMG (2018) Dengue virus in Aedes aegypti and Aedes albopictus in urban areas in the state of Rio Grande do Norte, Brazil: Importance of virological and entomological surveillance. PLoS ONE 13(3):1–11

    Article  Google Scholar 

  • Mellor PS (2000) Replication of arboviruses in insect vectors. Journal of Comparative Pathology 123(4):231–247

    Article  CAS  Google Scholar 

  • Mukhopadhyay S, Kuhn RJ, Rossmann MG (2005) A structural perspective of the flavivirus life cycle. Nature Reviews Microbiology 3(1):13–22

    Article  CAS  Google Scholar 

  • Nunes PCG, Daumas RP, Sánchez-Arcila JC, Nogueira RMR, Horta MAP, Santos FB (2019) 30 years of fatal dengue cases in Brazil: a review. BMC Public Health 19(329):1–11

    Google Scholar 

  • Oliveira DB, Machado G, Almeida GMF, Ferreira PCP, Bonjardim CA, Trindade GS, Abrahão JS, Kroon EG (2016) Infection of the central nervous system with Dengue virus 3 genotype I causing neurological manifestations in Brazil. Revista Da Sociedade Brasileira De Medicina Tropical 49(1):125–129

    Article  Google Scholar 

  • Pessanha JEM, Caiaffa WT, Cecílio AB, Iani FCM, Araujo SC, Nascimento JC, Kroon EG, Proietti FA, Arias JR (2011) Cocirculation of two Dengue virus serotypes in individual and pooled samples of Aedes aegypti and Aedes albopictus larvae. Revista Da Sociedade Brasileira De Medicina Tropical 44(1):103–105

    Article  Google Scholar 

  • Posada D (2011) jModelTest: phylogenetic model averaging. https://code.google.com/p/jmodeletest2/ [accessed June 24, 2018].

  • Secretaria de Vigilância em Saúde/ Ministério da Saúde (SVS/MS) (2013) Levantamento Rápido de Índices para Aedes Aegypti (LIRAa) para vigilância entomológica do Aedes aegypti no Brasil: metodologia para avaliação dos índices de Breteau e Predial e tipo de recipientes. Brasília: Ministério da Saúde. https://bvsms.saude.gov.br/bvs/publicacoes/manual_liraa_2013.pdf [accessed Oct 4, 2021].

  • Secretaria de Vigilância em Saúde/ Ministério da Saúde (SVS/MS) (2020) Óbito por arboviroses no Brasil, 2008 a 2019. Boletim Epidemiológico 33, v.51. https://antigo.saude.gov.br/images/pdf/2020/August/21/Boletim-epidemiologico-SVS-33.pdf [accessed Oct 30, 2020].

  • Sedda L, Vilela APP, Aguiar ERGR, Gaspar CHP, Gonçalves ANA, Olmo RP, Silva ATS, Silveira LC, Eiras AE, Drumond BP, Kroon EG, Marques JT (2018) The spatial and temporal scales of local Dengue virus transmission in natural settings: a retrospective analysis. Parasites & Vectors 11(79):1–14

    Google Scholar 

  • Souza KPR, Silva EG, Rocha ESO, Figueiredo LB, Almeida-Leite CM, Arantes RM, Assis Silva Gomes J, Ferreira GP, de Oliveira JG, Kroon EG, Campos MA (2013) Nitric oxide synthase expression correlates with death in an experimental mouse model of dengue with CNS involvement. Virology Journal 10(267):1–10

    Google Scholar 

  • Thongrungkiat S, Maneekan P, Wasinpiyamongkol L, Prummongkol S (2011) Prospective field study of transovarial dengue-virus transmission by two different forms of Aedes aegypti in an urban area of Bangkok, Thailand. Journal of Vector Ecology 36(1):147–152

    Article  Google Scholar 

  • Urdaneta L, Herrera F, Pernalete M, Zoghbi N, Rubio-Palis Y, Barrios R, Rivero J, Comach G, Jimézes M, Salcedo M (2005) Detection of Dengue viruses in field-caught Aedes aegypti (Diptera: Culicidae) in Maracay, Aragua state, Venezuela by type-specific polymerase chain reaction. Infection, Genetics and Evolution 5(2):177–184

    Article  CAS  Google Scholar 

  • Vilela APP, Figueiredo LB, Santos JR, Eiras AE, Bonjardim CA, Ferreira PCP, Kroon EG (2010) Dengue virus 3 genotype I in Aedes aegypti mosquitoes and eggs, Brazil, 2005–2006. Emerging Infectious Diseases 16(6):989–992

    Article  Google Scholar 

  • Weaver SC, Vasilakis N (2009) Molecular evolution of dengue viruses: contributions of phylogenetics to understanding the history and epidemiology of the preeminent arboviral disease. Infection, Genetics and Evolution 9(4):523–540

    Article  CAS  Google Scholar 

  • World Health Organization (WHO) (2020) Dengue and severe dengue. https://www.who.int/news-room/fact-sheets/detail/dengue-and-severe-dengue [accessed Dec 20, 2020].

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Acknowledgements

To the Secretaria Municipal de Saúde da Prefeitura de Contagem, especially endemic control agents from the Eldorado health district, Marco Túlio de Oliveira and Dr. Valdelaine Etelvina Miranda de Araújo. We also thank Dr. Álvaro Eiras for the BG traps. This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) and Ministério da Saúde, DECIT.

Funding

Funding was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico, Ministerio da Saúde, DECIT, Fundação de Amparo à Pesquisa do Estado de Minas Gerais, and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior.

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Authors and Affiliations

  1. Departamento de Tecnologia e Inspeção de Produtos de Origem Animal, Escola de Veterinária, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil

    Elisa Helena Paz Andrade

  2. Laboratório de Vírus, Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil

    Leandra Barcelos Figueiredo, Júlio César Câmara Rosa & Erna Geessien Kroon

  3. Plataforma Científica Pasteur-USP, Universidade de São Paulo, São Paulo, SP, Brazil

    Ana Paula Pessoa Vilela

  4. Secretaria de Saúde, Prefeitura Municipal de Contagem, Contagem, MG, Brazil

    Hassan Melo Zibaoui

Authors
  1. Elisa Helena Paz Andrade
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  2. Leandra Barcelos Figueiredo
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  3. Ana Paula Pessoa Vilela
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  4. Júlio César Câmara Rosa
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  5. Hassan Melo Zibaoui
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  6. Erna Geessien Kroon
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Correspondence to Erna Geessien Kroon.

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Andrade, E.H.P., Figueiredo, L.B., Vilela, A.P.P. et al. Virological Surveillance of Aedes aegypti Vectors Identifies All Four Dengue Serotypes in a Hyperendemic Region. EcoHealth 19, 75–84 (2022). https://doi.org/10.1007/s10393-022-01583-x

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  • DOI: https://doi.org/10.1007/s10393-022-01583-x

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