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. 2019;8(1):1668-1678.
doi: 10.1080/22221751.2019.1689797.

Zika virus threshold determines transmission by European Aedes albopictus mosquitoes

Affiliations

Zika virus threshold determines transmission by European Aedes albopictus mosquitoes

Marie Vazeille et al. Emerg Microbes Infect. 2019.

Abstract

Since its emergence in Yap Island in 2007, Zika virus (ZIKV) has affected all continents except Europe. Despite the hundreds of cases imported to European countries from ZIKV-infested regions, no local cases have been reported in localities where the ZIKV-competent mosquito Aedes albopictus is well established. Here we analysed the vector competence of European Aedes (aegypti and albopictus) mosquitoes to different genotypes of ZIKV. We demonstrate that Ae. albopictus from France was less susceptible to the Asian ZIKV than to the African ZIKV. Critically we show that effective crossing of anatomical barriers (midgut and salivary glands) after an infectious blood meal depends on a viral load threshold to trigger: (i) viral dissemination from the midgut to infect mosquito internal organs and (ii) viral transmission from the saliva to infect a vertebrate host. A viral load in body ≥4800 viral copies triggered dissemination and ≥12,000 viral copies set out transmission. Only 27.3% and 18.2% of Ae. albopictus Montpellier mosquitoes meet respectively these two criteria. Collectively, these compelling results stress the poor ability of Ae. albopictus to sustain a local transmission of ZIKV in Europe and provide a promising tool to evaluate the risk of ZIKV transmission in future outbreaks.

Keywords: Aedes albopictus; Europe; Zika; arbovirus; epidemic potential.

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Conflict of interest statement

No potential conflict of interest was reported by the authors.

Figures

Figure 1.
Figure 1.
Infection, dissemination and transmission rates of Aedes albopictus Corsica (a, b, c) and Montpellier (d, e, f), 7, 14, 21 days after exposure to an infectious blood meal containing ZIKV (Cambodia, Dakar and Martinique) provided at a titer of 107 TCID50/mL. IR, proportion of mosquitoes with infected body (abdomen plus thorax) among examined mosquitoes; DR, proportion of mosquitoes with virus detected in head among mosquitoes with infected body; TR, proportion of mosquitoes with virus detected in saliva among mosquitoes with infected head. **, p  0.01; ***, p  0.001.
Figure 2.
Figure 2.
Infection, dissemination and transmission rates of Aedes aegypti Funchal (a, b, c) and Haiti (d, e, f), 7, 14, 21 days after exposure to an infectious blood meal containing ZIKV (Cambodia, Dakar and Martinique) provided at a titer of 107 TCID50/mL. IR, proportion of mosquitoes with infected body (abdomen plus thorax) among examined mosquitoes; DR, proportion of mosquitoes with virus detected in head among mosquitoes with infected body; TR, proportion of mosquitoes with virus detected in saliva among mosquitoes with infected head. *, p < 0.05; **, p  0.01; ***, p  0.001.
Figure 3.
Figure 3.
Viral loads in mosquito body according to mosquito species (a) and viral dissemination status (b). Bodies (abdomen plus thorax) were homogenized and supernatants were titrated on Vero cells. Seven days after, viral copies were detected by CPE after staining with crystal violet.
Figure 4.
Figure 4.
ROC curve to identify mosquitoes capable of disseminating the virus according to the viral load in body.
Figure 5.
Figure 5.
Viral loads in mosquito heads according to mosquito species (a) and correlation between viral loads in bodies and heads (b).
Figure 6.
Figure 6.
Viral loads in mosquito bodies (a) and heads (b) according to viral transmission status.
Figure 7.
Figure 7.
Infection, dissemination and transmission rates of Aedes aegypti (AAFUNCHAL and AAHAITI) and Aedes albopictus (ALCORSICA and ALMONTPELLIER), 14 days after infection with ZIKV Martinique provided at a titer of 107 TCID50/mL. Body (Abdomen plus thorax), head and saliva were titrated on Vero cells to evaluate respectively infection, dissemination and transmission rates (rectangle in red). The mean number of viral particles is provided under each rectangle. The proportion of mosquitoes that meet the two criteria: ≥4800 viral copies and ≥12,000 viral copies in body needed to trigger dissemination and transmission respectively, were presented for each mosquito population.

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Grants and funding

This study was supported by the European Union’s Horizon 2020 research and innovation program (10.13039/501100007601/) under ZIKAlliance grant agreement no. 734548. It was partly funded by the French Government’s Investissement d’Avenir program, Laboratoire d’Excellence “Integrative Biology of Emerging Infectious Diseases” (grant n°ANR-10-LABX-62-IBEID, 10.13039/501100001665 to A-BF), the European Union's Horizon 2020 research and innovation program under grant agreement no. 731060 (Infravec2, Research Infrastructures for the control of vector-borne diseases; http://infravec2.eu/), and the European Union’s Horizon 2020 research and innovation program under EVAg grant agreement no. 653316 (https://www.european-virus-archive.com/).

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