Tropism of Bluetongue Virus in Culicoides midges

Arthropod-borne viruses (arboviruses) cause diseases of significant consequence to human and animal health. The aspect of the lifecycle that distinguishes an arbovirus from another viral group, is the requirement for replication in an arthropod vector and vertebrate host. Culicoides midges (order: Diptera; family: Ceratopogonidae) transmit several arboviral diseases of economic importance including bluetongue virus (BTV), a double-stranded RNA virus within the genus Orbivirus (family: Reoviridae).

The ability of an arbovirus, such as BTV, to replicate, disseminate and be transmitted to a susceptible host is determined by the interaction between extrinsic factors, such as the titre of ingested virus, and intrinsic factors such as the particular viral and vector genotype. This process is poorly understood. Here, data are presented to address this, describing BTV infection and replication in a model species, Culicoides sonorensis.

The percentages of infected cells were objectively determined in insect tissues using automated image classification. BTV infected cells of the posterior midgut and the number of cells infected were viral strain and dose-dependent and correlated with infection rate. Virus replicated to high levels in the compound eyes, fat body and epithelial cells. The brain and other neural tissues were infected at later times tested, coinciding with the expected time of BTV transmission. Viral RNA and antigen were undetectable in the salivary glands and oocytes, but were detected at high prevalence in the mouthparts.

These data show, for the first time, that Culicoides-borne arboviruses may exploit an alternative mechanism for transmission to a host than that used by mosquito-borne arboviruses. BTV may be transmitted directly from the mouthparts, without requiring the ability to replicate in the salivary glands.