Laboratory transmission potential of British mosquitoes for equine arboviruses

Abstract

Background: There has been no evidence of transmission of mosquito-borne arboviruses of equine or human health concern to date in the UK. However, in recent years there have been a number of outbreaks of viral diseases spread by vectors in Europe. These events, in conjunction with increasing rates of globalisation and climate change, have led to concern over the future risk of mosquito-borne viral disease outbreaks in northern Europe and have highlighted the importance of being prepared for potential disease outbreaks. Here we assess several UK mosquito species for their potential to transmit arboviruses important for both equine and human health, as measured by the presence of viral RNA in saliva at different time points after taking an infective blood meal. Results: The following wild-caught British mosquitoes were evaluated for their potential as vectors of zoonotic equine arboviruses: Ochlerotatus detritus for Venezuelan equine encephalitis virus (VEEV) and Ross River virus (RRV), and Culiseta annulata and Culex pipiens for Japanese encephalitis virus (JEV). Production of RNA in saliva was demonstrated at varying efficiencies for all mosquito-virus pairs. Ochlerotatus detritus was more permissive for production of RRV RNA in saliva than VEEV RNA. For RRV, 27.3% of mosquitoes expectorated viral RNA at 7 days post-infection when incubated at 21 °C and 50% at 24 °C. Strikingly, 72% of Cx. pipiens produced JEV RNA in saliva after 21 days at 18 °C. For some mosquito-virus pairs, infection and salivary RNA titres reduced over time, suggesting unstable infection dynamics. Conclusions: This study adds to the number of Palaearctic mosquito species that demonstrate expectoration of viral RNA, for arboviruses of importance to human and equine health. This work adds to evidence that native mosquito species should be investigated further for their potential to vector zoonotic mosquito-borne arboviral disease of equines in northern Europe. The evidence that Cx. pipiens is potentially an efficient laboratory vector of JEV at temperatures as low as 18 °C warrants further investigation, as this mosquito is abundant in cooler regions of Europe and is considered an important vector for West Nile Virus, which has a comparable transmission ecology.

Temperate conditions restrict Japanese encephalitis virus infection to the mid-gut and prevents systemic dissemination in Culex pipiens mosquitoes

“…Consequently, investigating how repeated transmission in vectors may impact viral evolution and epidemiology with JEV warrants further investigation. Interestingly, Chapman et al 31 reported the recovery of JEV RNA from 72% of infected C. pipiens saliva samples at 18 °C, whereas we did not recover any JEV RNA in saliva at 20 °C. It is important to note that Chapman et al collected saliva at day 21 and the infection paradigm used JEV strain CNS138-11, which is representative of JEV genotype II 37 .…”

“…This corroborates experimental findings from other Cx. pipiens populations from the UK, Europe and Asia [29][30][31] . Given that we recorded such a marked increase in infection and dissemination prevalence at 25 °C it is likely that the limiting temperature at which Cx.…”

“…It is therefore unclear from these observations whether the restriction to the midgut was a result of active anti-viral control by the mosquitoes or the lower temperature alone restricting virus replication 49 . It is possible that an increase in temperature, or an increase in the duration of the experiment 31 could trigger further virus replication and escape from the midgut. These results highlight the important role of midgut cells in mosquito-resistance and control of arboviruses, especially JEV infection in this model, which has been shown for other pathogens, including other Flaviviridae 48 , 50 .…”

“…In addition recent investigations have confirmed that Cx. pipiens from France 29 , China 30 and the UK 31 are competent to transmit JEV.…”

Mosquito Vector Competence for Japanese Encephalitis Virus

“…pipiens to mice [ 90 ], and determine possible transmission by detecting JEV in the saliva of the mosquitoes as early as 7 dpi for a certain JEV isolate from China [ 94 ], and at 21 dpi in Cx . pipiens from the UK [ 95 ]. The virus was also found in the saliva of Cx .…”