Bluetongue virus changes the emission of volatile organic chemicals in the body odour of sheep and cattle during infection

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Mammals, including humans, constantly emit hundreds of volatile organic chemicals (VOCs) as part of body odour and their individual composition alters in response to underlying biological and environmental influences. These chemicals will also change in response to diseases and infections. Innovative new technologies are being used to explore odour-based biomarkers in breath, skin emissions and excretions as diagnostics tools for the early detection of difficult-to-diagnose conditions like cancer and tuberculosis. The emission of VOCs is of particular importance for vector-borne pathogens such as the malaria parasite or arthropod-borne viruses (arboviruses) such as Zika virus, as insects who transmit these pathogens use specific chemicals in body odour (semiochemicals) as one way of finding their host. An emerging field of research is investigating how vector-borne pathogens modify the body odour of infected hosts to identify if infection-induced changes to body odour semiochemicals subsequently alter the attraction of insect vectors. Studies based on human: mosquito: malaria interactions are at the forefront of this research and recent high-profile outcomes have reported that mosquitoes are more attracted to infected individuals. Most intriguingly vector mosquitoes might be specifically attracted to those infection stages of the parasite that will enhance successful transmission. Despite the overall importance surprising little is known in regards to the effect of arbovirus infections on body odour modification and subsequent insect vector attraction. Most arbovirus infections of humans and animals are acute and characterised by shorter periods of virus presence in the blood (viraemia), making the collection of body odour emissions during natural infections across rapidly changing stages of infection challenging. In contrast, while the development of mouse models of infection offers flexibility and a vast associated array of interrogative tools, they are limited in their relevance to natural infections. Arboviruses cause highly important diseases also in livestock. Culicoides-borne viruses such as bluetongue virus (BTV) can cause devastating disease in some species of ruminants and are a current major threat to the UK agriculture sector due to ongoing outbreaks in continental Europe. Combining the unique expertise of all project partners we have created a novel and flexible infection system that remains relevant to the real world and translatable to field application. In a proof-of-concept study we will investigate the hypothesis that BTV infection changes VOC profiles in the body odour of the main natural hosts, cattle and sheep. Detected BTV-induced host odour changes can subsequently be assessed for their potential to modify the attraction of insect vectors as well as highlight opportunities for novel diagnostic tools. BTV causes more severe disease in sheep than in cattle despite an equally high level of virus in the blood. Therefore this study system will also determine if odour based diagnostic technology can be developed to detect viral infections even in the absence of clinical signs. The latter is of vital importance as odour-based detection of non-diseased but infected individuals could transform both pen-side diagnostic systems and control measures such as repellent and attractant chemicals available for insect vector control. Study outcomes will immediately improve our understanding of BTV transmission and highlight opportunities for targeted control of Culicoides vectors. Importantly study results can in the future be transferred to other highly important viral pathogens of livestock and identify if different virus species induce specific odour changes. Demonstrating this will be of vital interest not only for other vector-borne viral diseases including those of humans, but also significantly advance the emerging field of odour-based detection of viral infections.