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Low vector competence in sylvatic mosquitoes limits Zika virus to initiate an enzootic cycle in South America.

ABSTRACT: Zika virus (ZIKV) has spread in the Americas since 2015 and the potential establishment of a sylvatic transmission cycle in the continent has been hypothesized. We evaluated vector competence of five sylvatic Neotropical mosquito species to two ZIKV isolates. Distinct batches of Haemagogus leucoceleanus, Sabethes albiprivus, Sabethes identicus, Aedes terrens and Aedes scapularis females were respectively orally challenged and inoculated intrathoracically with ZIKV. Orally challenged mosquitoes were refractory or exhibited low infection rates. Viral dissemination was detected only in Hg. leucocelaenus, but with very low rates. Virus was not detected in saliva of any mosquito orally challenged with ZIKV, regardless of viral isolate and incubation time. When intrathoracically injected, ZIKV disseminated in high rates in Hg. leucocelaenus, Sa. identicus and Sa. albpiprivus, but low transmission was detected in these species; very low dissemination and no transmission was detected in Ae. terrens and Ae. scapularis. Together these results suggest that genetically determined tissue barriers, especially in the midgut, play a vital role in inhibiting ZIKV for transmission in the tested sylvatic mosquito species. Thus, an independent enzootic transmission cycle for ZIKV in South America is very unlikely.

SUBMITTER: Fernandes RS

PROVIDER: S-EPMC6934573 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Low vector competence in sylvatic mosquitoes limits Zika virus to initiate an enzootic cycle in South America.

Fernandes Rosilainy S RS Bersot Maria I MI Castro Marcia G MG Telleria Erich Loza EL Ferreira-de-Brito Anielly A Raphael Lidiane M LM Bonaldo Myrna C MC Lourenço-de-Oliveira Ricardo R

Scientific reports 20191227 1

Zika virus (ZIKV) has spread in the Americas since 2015 and the potential establishment of a sylvatic transmission cycle in the continent has been hypothesized. We evaluated vector competence of five sylvatic Neotropical mosquito species to two ZIKV isolates. Distinct batches of Haemagogus leucoceleanus, Sabethes albiprivus, Sabethes identicus, Aedes terrens and Aedes scapularis females were respectively orally challenged and inoculated intrathoracically with ZIKV. Orally challenged mosquitoes w ...[more]

PMID: 31882976

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Project description:BACKGROUND:Vector-borne diseases are a major public health concern and cause significant morbidity and mortality. Zika virus (ZIKV) is the etiologic agent of a massive outbreak in the Americas that originated in Brazil in 2015 and shows a strong association with congenital ZIKV syndrome in newborns. Cache Valley virus (CVV) is a bunyavirus that causes mild to severe illness in humans and ruminants. In this study, we investigated the vector competence of Virginia mosquitoes for ZIKV and CVV to explore their abilities to contribute to potential outbreaks. METHODS:To determine vector competence, mosquitoes were fed a blood meal comprised of defibrinated sheep blood and virus. The presence of midgut or salivary gland barriers to ZIKV infection were determined by intrathoracic inoculation vs oral infection. After 14-days post-exposure, individual mosquitoes were separated into bodies, legs and wings, and saliva expectorant. Virus presence was detected by plaque assay to determine midgut infection, dissemination, and transmission rates. RESULTS:Transmission rates for Ae. albopictus orally infected (24%) and intrathoracically inoculated (63%) with ZIKV was similar to Ae. aegypti (48% and 71%, respectively). Transmission rates of ZIKV in Ae. japonicus were low, and showed evidence of a midgut infection barrier demonstrated by low midgut infection and dissemination rates from oral infection (3%), but increased transmission rates after intrathoracic inoculation (19%). Aedes triseriatus was unable to transmit ZIKV following oral infection or intrathoracic inoculation. CVV transmission was dose-dependent where mosquitoes fed high titer (ht) virus blood meals developed higher rates of midgut infection, dissemination, and transmission compared to low titer (lt) virus blood meals. CVV was detected in the saliva of Ae. albopictus (ht: 68%, lt: 24%), Ae. triseriatus (ht: 52%, lt: 7%), Ae. japonicus (ht: 22%, lt: 0%) and Ae. aegypti (ht: 10%; lt: 7%). Culex pipiens and Cx. restuans were not competent for ZIKV or CVV. CONCLUSIONS:This laboratory transmission study provided further understanding of potential ZIKV and CVV transmission cycles with Aedes mosquitoes from Virginia. The ability for these mosquitoes to transmit ZIKV and CVV make them a public health concern and suggest targeted control programs by mosquito and vector abatement districts.

Project description:BackgroundZika virus is an emerging pathogen of global importance. It has been responsible for recent outbreaks in the Americas and in the Pacific region. This study assessed five different mosquito species from the temperate climatic zone in Australia and included Aedes albopictus as a potentially invasive species.MethodsMosquitoes were orally challenged by membrane feeding with Zika virus strain of Cambodia 2010 origin, belonging to the Asian clade. Virus infection and dissemination were assessed by quantitative PCR on midgut and carcass after dissection. Transmission was assessed by determination of cytopathogenic effect of saliva (CPE) on Vero cells, followed by determination of 50% tissue culture infectious dose (TCID50) for CPE positive samples. Additionally, the presence of Wolbachia endosymbiont infection was assessed by qPCR and standard PCR.ResultsCulex mosquitoes were found unable to present Zika virus in saliva, as demonstrated by molecular as well as virological methods. Aedes aegypti, was used as a positive control for Zika infection and showed a high level of virus infection, dissemination and transmission. Local Aedes species, Ae. notoscriptus and, to a lesser degree, Ae. camptorhynchus were found to expel virus in their saliva and contained viral nucleic acid within the midgut. Molecular assessment identified low or no dissemination for these species, possibly due to low virus loads. Ae. albopictus from Torres Strait islands origin was shown as an efficient vector. Cx quinquefasciatus was shown to harbour Wolbachia endosymbionts at high prevalence, whilst no Wolbachia was found in Cx annulirostris. The Australian Ae. albopictus population was shown to harbour Wolbachia at high frequency.ConclusionsThe risk of local Aedes species triggering large Zika epidemics in the southern parts of Australia is low. The potentially invasive Ae. albopictus showed high prevalence of virus in the saliva and constitutes a potential threat if this mosquito species becomes established in mainland Australia. Complete risk analysis of Zika transmission in the temperate zone would require an assessment of the impact of temperature on Zika virus replication within local and invasive mosquito species.

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Low vector competence in sylvatic mosquitoes limits Zika virus to initiate an enzootic cycle in South America.

Publications

Low vector competence in sylvatic mosquitoes limits Zika virus to initiate an enzootic cycle in South America.

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