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. 2016 Jul 8:16:318.
doi: 10.1186/s12879-016-1666-0.

Competitive advantage of a dengue 4 virus when co-infecting the mosquito Aedes aegypti with a dengue 1 virus

Marie Vazeille  1 , Pascal Gaborit  2 , Laurence Mousson  1 , Romain Girod  2 , Anna-Bella Failloux  3
Affiliations

Competitive advantage of a dengue 4 virus when co-infecting the mosquito Aedes aegypti with a dengue 1 virus

Marie Vazeille et al. BMC Infect Dis. .

Abstract

Background: Dengue viruses (DENV) are comprised in four related serotypes (DENV-1 to 4) and are critically important arboviral pathogens affecting human populations in the tropics. South American countries have seen the reemergence of DENV since the 1970's associated with the progressive re-infestation by the mosquito vector, Aedes aegypti. In French Guiana, DENV is now endemic with the co-circulation of different serotypes resulting in viral epidemics. Between 2009 and 2010, a predominant serotype change occurred from DENV-1 to DENV-4 suggesting a competitive displacement. The aim of the present study was to evaluate the potential role of the mosquito in the selection of the new epidemic serotype.

Methods: To test this hypothesis of competitive displacement of one serotype by another in the mosquito vector, we performed mono- and co-infections of local Ae. aegypti collected during the inter-epidemic period with both viral autochthonous epidemic serotypes and compared infection, dissemination and transmission rates. We performed oral artificial infections of F1 populations in BSL-3 conditions and analyzed infection, dissemination and transmission rates.

Results: When two populations of Ae. aegypti from French Guiana were infected with either serotype, no significant differences in dissemination and transmission were observed between DENV-1 and DENV-4. However, in co-infection experiments, a strong competitive advantage for DENV-4 was seen at the midgut level leading to a much higher dissemination of this serotype. Furthermore only DENV-4 was present in Ae. aegypti saliva and therefore able to be transmitted.

Conclusions: In an endemic context, mosquito vectors may be infected by several DENV serotypes. Our results suggest a possible competition between serotypes at the midgut level in co-infected mosquitoes leading to a drastically different transmission potential and, in this case, favoring the competitive displacement of DENV-1 by DENV-4. This phenomenon was observed despite a similar replicative fitness in mono-infections conditions.

Keywords: Aedes aegypti; Co-infection; Competitive interactions; Dengue.

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Figures

Fig. 1
Fig. 1
Mono infections of Aedes aegypti. Mono-infections with DENV-1 or DENV-4 of two populations of Aedes aegypti (CEN and MAD) collected in French Guiana in 2009. (a) Dissemination efficiency 14 days after DENV-infected blood-meals provided at a titer of 105 or 106 ffu/mL. (b) Dissemination efficiency and (c) transmission rate at different days after oral infection with DENV-1 or DENV-4 provided at 106 ffu/mL. Error bars show confidence intervals (95 %). In brackets, the number of mosquitoes tested
Fig. 2
Fig. 2
Coinfection of Aedes aegypti. Infection, dissemination and transmission rates in Ae. aegypti CEN population, 21 days after oral exposure to co-infected blood-meal DENV-1/DENV-4 provided at 106 ffu/mL for each virus. Viral RNA was detected by qRT-PCR. Error bars show confidence intervals (95 %). In brackets, the number of mosquitoes tested
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