Differential Vector Competency of Aedes albopictus Populations from the Americas for Zika Virus

Sasha R. Azar Department of Pathology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, Texas;
Center for Tropical Diseases, University of Texas Medical Branch, Galveston, Texas;
Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas;

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Christopher M. Roundy Department of Pathology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, Texas;
Center for Tropical Diseases, University of Texas Medical Branch, Galveston, Texas;
Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas;

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Shannan L. Rossi Department of Pathology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, Texas;
Center for Tropical Diseases, University of Texas Medical Branch, Galveston, Texas;

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Jing H. Huang Department of Pathology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, Texas;
Center for Tropical Diseases, University of Texas Medical Branch, Galveston, Texas;

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Grace Leal Department of Pathology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, Texas;
Center for Tropical Diseases, University of Texas Medical Branch, Galveston, Texas;

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Ruimei Yun Department of Pathology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, Texas;
Center for Tropical Diseases, University of Texas Medical Branch, Galveston, Texas;

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Ildefonso Fernandez-Salas Instituto Nacional de Salud Pública, Centro Regional de Salud Pública, Tapachula, Chiapas, México;

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Christopher J. Vitek University of Texas Rio Grande Valley, Edinburg, Texas;

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Igor A. D. Paploski Centro de Pesquisas Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Candeal, Salvador, Brazil;
Instituto de Saúde Coletiva, Universidade Federal da Bahia, Salvador, Brazil;

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Pamela M. Stark Mosquito and Vector Control Division, Harris County Public Health, Houston, Texas;

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Jeremy Vela Mosquito and Vector Control Division, Harris County Public Health, Houston, Texas;

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Mustapha Debboun Mosquito and Vector Control Division, Harris County Public Health, Houston, Texas;

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Martin Reyna Mosquito and Vector Control Division, Harris County Public Health, Houston, Texas;

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Uriel Kitron Population Biology, Ecology, and Evolution Graduate Program, Graduate Division of Biological and Biomedical Sciences, Department of Environmental Sciences, Emory University, Atlanta, Georgia;

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Guilherme S. Ribeiro Centro de Pesquisas Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Candeal, Salvador, Brazil;
Instituto de Saúde Coletiva, Universidade Federal da Bahia, Salvador, Brazil;

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Kathryn A. Hanley Department of Biology, New Mexico State University, Las Cruces, New Mexico

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Nikos Vasilakis Department of Pathology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, Texas;
Center for Tropical Diseases, University of Texas Medical Branch, Galveston, Texas;

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Scott C. Weaver Department of Pathology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, Texas;
Center for Tropical Diseases, University of Texas Medical Branch, Galveston, Texas;
Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas;

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To evaluate the potential role of Aedes albopictus (Skuse) as a vector of Zika virus (ZIKV), colonized mosquitoes of low generation number (≤ F5) from Brazil, Houston, and the Rio Grande Valley of Texas engorged on viremic mice infected with ZIKV strains originating from Senegal, Cambodia, Mexico, Brazil, or Puerto Rico. Vector competence was established by monitoring infection, dissemination, and transmission potential after 3, 7, and 14 days of extrinsic incubation. Positive saliva samples were assayed for infectious titer. Although all three mosquito populations were susceptible to all ZIKV strains, rates of infection, dissemination, and transmission differed among mosquito and virus strains. Aedes albopictus from Salvador, Brazil, were the least efficient vectors, demonstrating susceptibility to infection to two American strains of ZIKV but failing to shed virus in saliva. Mosquitoes from the Rio Grande Valley were the most efficient vectors and were capable of shedding all three tested ZIKV strains into saliva after 14 days of extrinsic incubation. In particular, ZIKV strain DakAR 41525 (Senegal 1954) was significantly more efficient at dissemination and saliva deposition than the others tested in Rio Grande mosquitoes. Overall, our data indicate that, while Ae. albopictus is capable of transmitting ZIKV, its competence is potentially dependent on geographic origin of both the mosquito population and the viral strain.

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Author Notes

Address correspondence to Nikos Vasilakis or Scott C. Weaver, University of Texas Medical Branch, 301 University Blvd., Galveston TX 77555-0609. E-mails: nivasila@utmb.edu or sweaver@utmb.edu
These authors contributed equally to this work.

Financial support: This work was supported by a pilot grant by the Institute for Human Infections and Immunity. NIH grants R24AI120942 and R01AI121452 (SCW), 1U01AI115577 (NV) and 1R15AI113628-01 (KAH), and grants from Brazilian National Council of Technological and Scientific Development (440891/2016-7 and 400830/2013-2) and the Coordination for the Improvement of Higher Education (440891/2016-7) (GSR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors have no conflicting financial interests.

Authors' addresses: Sasha R. Azar, Christopher M. Roundy, and Scott C. Weaver, Department of Pathology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, TX, Center for Tropical Diseases, University of Texas Medical Branch, Galveston, TX, and Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, E-mails: srazar@utmb.edu, cmroundy@utmb.edu, and sweaver@utmb.edu. Shannan L. Rossi, Jing H. Huang, Grace Leal, Ruimei Yun, and Scott C. Weaver, Department of Pathology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, TX, and Center for Tropical Diseases, University of Texas Medical Branch, Galveston, TX, E-mails: slrossi@utmb.edu, jhhuang@utmb.edu, grleal@utmb.edu, ruyun@utmb.edu, and nivasila@utmb.edu. Ildefonso Fernandez-Salas, Instituto Nacional de Salud Pública, Centro Regional de Salud Pública, Tapachula, Chiapas, México, E-mail: ildefonso.fernandez@insp.mxhiapas. Christopher J. Vitek, University of Texas Rio Grande Valley, Edinburg, TX, E-mail: christopher.vitek@utrgv.edu. Igor A. D. Paploski and Guilherme S. Ribeiro, Centro de Pesquisas Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Candeal, Salvador, Brazil, and Instituto de Saúde Coletiva, Universidade Federal da Bahia, Salvador, Brazil, E-mails: igorufprmv@gmail.com and gsribeiro@gmail.com. Pamela M. Stark, Jeremy Vela, Mustapha Debboun, and Martin Reyna, Harris County Public Health Mosquito and Vector Control Division, Houston, TX, E-mails: pstark@hcphes.org, jvela@hcphes.org, mdebboun@hcphes.org, and mreyna@hcphes.org. Uriel Kitron, Population Biology, Ecology, and Evolution Graduate Program, Graduate Division of Biological and Biomedical Sciences, Department of Environmental Studies, Emory University, Atlanta, GA, E-mail: ukitron@emory.edu. Kathryn A. Hanley, Department of Biology, New Mexico State University, Las Cruces, New Mexico, E-mail: khanley@nmsu.edu.

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