Quantifying and modelling the acquisition and retention of lumpy skin disease virus by haematophagus insects reveals clinically but not subclinically-affected cattle are promoters of viral transmission and key targets for control of disease outbreaks

Beatriz Sanz-Bernardo, Ismar R Haga, Najith Wijesiriwardana, Sanjay Basu, Will Larner, Adriana V Diaz, Zoë Langlands, Eric Denison, Joanne Stoner, Mia White, Christopher Sanders, Philippa C Hawes, Anthony J Wilson, John Atkinson, Carrie Batten, Luke Alphey, Karin E Darpel, Simon Gubbins, Philippa M Beard

Research output: Contribution to journalArticlepeer-review

Abstract

Lumpy skin disease virus (LSDV) is a vector-transmitted poxvirus that causes disease in cattle. Vector species involved in LSDV transmission and their ability to acquire and transmit the virus are poorly characterised. Using a highly representative bovine experimental model of lumpy skin disease we fed four model vector species (Aedes aegypti, Culex quinquefasciatus, Stomoxys calcitrans and Culicoides nubeculosus) on LSDV-inoculated cattle in order to examine their acquisition and retention of LSDV. Subclinical disease was a more common outcome than clinical disease in the inoculated cattle. Importantly, the probability of vectors acquiring LSDV from a subclinical animal (0.006) was very low compared to acquisition from a clinical animal (0.23), meaning an insect feeding on a subclinical animal was 97% less likely to acquire LSDV than one feeding on a clinical animal. All four potential vector species studied acquired LSDV at a similar rate from the host, but Aedes aegypti and Stomoxys calcitrans retained the virus for a longer time, up to 8 days. There was no evidence of virus replication in the vector, consistent with mechanical rather than biological transmission. The parameters obtained in this study were combined with data from studies of LSDV transmission and vector life history parameters to determine the basic reproduction number of LSDV in cattle mediated by each of the model species. This was highest for Stomoxys calcitrans (19.1), C. nubeculosus (7.1), and Ae. aegypti (2.4), indicating these three species are potentially efficient transmitters of LSDV, which can be used to inform LSD control programmes.Importance: Lumpy skin disease virus (LSDV) causes a severe systemic disease characterised by cutaneous nodules in cattle. LSDV is a rapidly emerging pathogen, having spread since 2012 into Europe and Russia, and across Asia. The vector-borne nature of LSDV transmission is believed to have promoted this rapid geographic spread of the virus, however a lack of quantitative evidence about LSDV transmission has hampered effective control of the disease during the current epidemic. Our research shows subclinical cattle play little part in virus transmission relative to clinical cattle, and reveals a low probability of virus acquisition by insects at the pre-clinical stage. We have also calculated the reproductive number of different insect species, therefore identifying efficient transmitters of LSDV. This information is of utmost importance, as it will help to define epidemiological control measures during LSDV epidemics and of particular consequence in resource-poor regions where LSD vaccination may be less than adequate.

Original languageEnglish
JournalJournal of Virology
Early online date10 Feb 2021
DOIs
Publication statusPublished - 12 Apr 2021

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