Vertical Transmission of Zika Virus (Flaviviridae, Flavivirus) in Amazonian Aedes aegypti (Diptera: Culicidae) Delays Egg Hatching and Larval Development of Progeny

Author:

Chaves Barbara Aparecida12,Junior Ademir Bentes Vieira1,Silveira Karine Renata Dias3,Paz Andreia da Costa1,Vaz Evelyn Beatriz da Costa1,Araujo Raphaela Guedes Pereira3,Rodrigues Nilton Barnabe3,Campolina Thais Bonifacio3,Orfano Alessandra da Silva3,Nacif-Pimenta Rafael3,Villegas Luis Eduardo Martinez3,Melo Fabrício Freire de4,Silva Breno de Mello5,Monteiro Wuelton Marcelo12,Guerra Maria das Graças Vale Barbosa12,Lacerda Marcus Vinicius Guimarães de16,Norris Douglas Eric7,Secundino Nagila Francinete Costa3,Pimenta Paulo Filemon Paolucci13

Affiliation:

1. Tropical Medicine Foundation Dr. Heitor Vieira Dourado, Manaus, Amazonas, Brazil

2. Amazonas State University, Minas Gerais, Belo Horizonte, Brazil

3. Laboratory of Medical Entomology, Rene Rachou Research Institute – FIOCRUZ, Minas Gerais, Belo Horizonte, Brazil

4. Multidisciplinary Health Institute, Federal University of Bahia, Bahia, Brazil

5. Department of Biological Sciences, Federal University of Ouro Preto, Minas Gerais, Ouro Preto, Brazil

6. Leonidas and Maria Deane Research institute – FIOCRUZ, Amazonas, Brazil

7. The Harry Feinstone Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD

Abstract

Abstract Zika virus (ZIKV) has emerged as a globally important arbovirus and has been reported from all states of Brazil. The virus is primarily transmitted to humans through the bite of an infective Aedes aegypti (Linnaeus, 1762) or Aedes albopictus (Skuse, 1895). However, it is important to know if ZIKV transmission also occurs from Ae. aegypti through infected eggs to her offspring. Therefore, a ZIKV and dengue virus (DENV) free colony was established from eggs collected in Manaus and maintained until the third–fourth generation in order to conduct ZIKV vertical transmission (VT) experiments which used an infectious bloodmeal as the route of virus exposure. The eggs from ZIKV-infected females were allowed to hatch. The resulting F1 progeny (larvae, pupae, and adults) were quantitative polymerase chain reaction (qPCR) assayed for ZIKV. The viability of ZIKV vertically transmitted to F1 progeny was evaluated by cultivation in C6/36 cells. The effects of ZIKV on immature development of Ae. aegypti was assessed and compared with noninfected mosquitoes. AmazonianAe. aegypti were highly susceptible to ZIKV infection (96.7%), and viable virus passed to their progeny via VT. Moreover, eggs from the ZIKV-infected mosquitoes had a significantly lower hatch rate and the slowest hatching. In addition, the larval development period was slower when compared to noninfected, control mosquitoes. This is the first study to illustrate VT initiated by oral infection of the parental population by using mosquitoes, which originated from the field and a ZIKV strain that is naturally circulating in-country. Additionally, this study suggests that ZIKV present in the Ae. aegypti can modify the mosquito life cycle. The data reported here suggest that VT of ZIKV to progeny from naturally infected females may have a critical epidemiological role in the dissemination and maintenance of the virus circulating in the vector.

Funder

Foundation of the Institute Oswaldo Cruz

Strategic Program for Supporting Health Research

Brazilian Council for Scientific and Technological Development

Program Science without Borders

INCT-Instituto Nacional de Ciencia e Tecnologia - Entomologia Molecular, Minas Gerais State Research Support Foundation

Amazonas State Research Support Foundation

Federal University of Bahia

CAPES

CNPq

FAPEAM

Publisher

Oxford University Press (OUP)

Subject

Infectious Diseases,Insect Science,General Veterinary,Parasitology

Reference27 articles.

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2. Brazilian Ministry of Health . 2017a. Monitoramento dos casos de dengue, febre de chikungunya e febre pelo vírus Zika até a Semana Epidemiológica 4, 2017 (Portuguese). http://combateaedes.saude.gov.br/images/pdf/2017-Dengue_Zika_Chikungunya-SE4.pdf.

3. Brazilian Ministry of Health . 2017b. Monitoramento integrado de alterações no crescimento e desenvolvimento relacionadas à infecção pelo vírus Zika e outras etiologias infecciosas, até a Semana Epidemiológica 18/2017 (Portuguese). http://portalarquivos.saude.gov.br/images/pdf/2017/junho/01/BE-2017-015-Monitoramento-integrado-de-alteracoes-no-crescimento-e-desenvolvimento.pdf.

4. Vertical transmission of key West dengue-1 virus by Aedes aegypti and Aedes albopictus (Diptera: Culicidae) mosquitoes from Florida;Buckner;J. Med. Entomol,2013

5. Differential susceptibilities of Aedes aegypti and Aedes albopictus from the Americas to Zika virus;Chouin-Carneiro;Plos Negl. Trop. Dis,2016

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