A Modeling Framework to Describe the Transmission of Bluetongue Virus within and between Farms in Great Britain

Background Recently much attention has been given to developing national-scale micro-simulation models for livestock diseases that can be used to predict spread and assess the impact of control measures. The focus of these models has been on directly transmitted infections with little attention given to vector-borne diseases such as bluetongue, a viral disease of ruminants transmitted by Culicoides biting midges. Yet BT has emerged over the past decade as one of the most important diseases of livestock. Methodology/Principal Findings We developed a stochastic, spatially-explicit, farm-level model to describe the spread of bluetongue virus (BTV) within and between farms. Transmission between farms was modeled by a generic kernel, which includes both animal and vector movements. Once a farm acquired infection, the within-farm dynamics were simulated based on the number of cattle and sheep kept on the farm and on local temperatures. Parameter estimates were derived from the published literature and using data from the outbreak of bluetongue in northern Europe in 2006. The model was validated using data on the spread of BTV in Great Britain during 2007. The sensitivity of model predictions to the shape of the transmission kernel was assessed. Conclusions/Significance The model is able to replicate the dynamics of BTV in Great Britain. Although uncertainty remains over the precise shape of the transmission kernel and certain aspects of the vector, the modeling approach we develop constitutes an ideal framework in which to incorporate these aspects as more and better data become available. Moreover, the model provides a tool with which to examine scenarios for the spread and control of BTV in Great Britain.

[1]  P. Mellor,et al.  Culicoides and the emergence of bluetongue virus in northern Europe. , 2009, Trends in microbiology.

[2]  P. Mellor,et al.  Bluetongue in Europe and the Mediterranean Basin: history of occurrence prior to 2006. , 2008, Preventive veterinary medicine.

[3]  P. Mellor,et al.  Bluetongue in Europe: vectors, epidemiology and climate change , 2008, Parasitology Research.

[4]  M. Gilbert,et al.  A wind density model to quantify the airborne spread of Culicoides species during north-western Europe bluetongue epidemic, 2006. , 2008, Preventive veterinary medicine.

[5]  E. A. Goodall,et al.  Society for veterinary epidemiology and preventive medicine. , 2000 .

[6]  Simon Gubbins,et al.  Assessing the risk of bluetongue to UK livestock: uncertainty and sensitivity analyses of a temperature-dependent model for the basic reproduction number , 2007, Journal of The Royal Society Interface.

[7]  S. Pacala,et al.  Modeling and analysis of stochastic invasion processes , 2000, Journal of mathematical biology.

[8]  Neil M Ferguson,et al.  Epidemiological inference for partially observed epidemics: the example of the 2001 foot and mouth epidemic in Great Britain. , 2009, Epidemics.

[9]  R. Marcus,et al.  Seasonal survival and expectation of infective life of Culicoides spp. (Diptera: Ceratopogonidae) in Israel, with implications for bluetongue virus transmission and a comparison of the parous rate in C. imicola from Israel and Zimbabwe. , 1985, Journal of medical entomology.

[10]  D Mollison,et al.  Dependence of epidemic and population velocities on basic parameters. , 1991, Mathematical biosciences.

[11]  S. Gubbins,et al.  Quantifying the Risk of Localised Animal Movement Bans for Foot-and-Mouth Disease , 2009, PloS one.

[12]  E. Schmidtmann,et al.  Environmental effects on vector competence and virogenesis of bluetongue virus in Culicoides: interpreting laboratory data in a field context. , 2004, Veterinaria italiana.

[13]  Christl A. Donnelly,et al.  The Foot-and-Mouth Epidemic in Great Britain: Pattern of Spread and Impact of Interventions , 2001, Science.

[14]  B Durand,et al.  A point pattern model of the spread of foot-and-mouth disease. , 2002, Preventive veterinary medicine.

[15]  P. Mellor,et al.  Oral Susceptibility to Bluetongue virus of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom , 2006, Journal of medical entomology.

[16]  W. Taylor The epidemiology of bluetongue. , 1986, Revue scientifique et technique.

[17]  R. May,et al.  Modelling vaccination strategies against foot-and-mouth disease , 2003, Nature.

[18]  C. Webb,et al.  Simulation of the options for a national control programme to eradicate scrapie from Great Britain. , 2005, Preventive veterinary medicine.

[19]  O. Francino,et al.  Biting Rates of Culicoides Midges (Diptera: Ceratopogonidae) on Sheep in Northeastern Spain in Relation to Midge Capture Using UV Light and Carbon Dioxide-Baited Traps , 2009, Journal of medical entomology.

[20]  S. Gubbins,et al.  Mortality and case fatality during the recurrence of BTV-8 in northern Europe in 2007 , 2007, Veterinary Record.

[21]  G. Roberts,et al.  A novel approach to real-time risk prediction for emerging infectious diseases: a case study in Avian Influenza H5N1. , 2009, Preventive veterinary medicine.

[22]  M. Birley,et al.  ESTIMATING THE SURVIVAL AND BITING OF HAEMATOPHAGUS INSECTS WITH PARTICULAR REFERENCE OF CULICOIDES OBOSLETUS GROUP (DIPTERA: CERATOPOGONIDAE) IN SOUTHERN ENGLAND , 1982 .

[23]  A. Tadmor,et al.  The comparative sensitivity of sheep and chicken embryos to bluetongue virus and observations on viraemia in experimentally infected sheep. , 1975, Australian veterinary journal.

[24]  A. Gerry,et al.  Comparison of bait cattle and carbon dioxide-baited suction traps for collecting Culicoides variipennis sonorensis (Diptera: Ceratopogonidae) and Culex quinquefasciatus (Diptera: Culicidae). , 1998, Journal of medical entomology.

[25]  R. E. Wheeler Statistical distributions , 1983, APLQ.

[26]  F. Monaco,et al.  Bluetongue virus isolations from midges belonging to the Obsoletus complex (Culicoides, Diptera: Ceratopogonidae) in Italy , 2005, Veterinary Record.

[27]  M. Evans Statistical Distributions , 2000 .

[28]  P. Mellor,et al.  Live attenuated bluetongue vaccine viruses in Dorset Poll sheep, before and after passage in vector midges (Diptera: Ceratopogonidae). , 2005, Vaccine.

[29]  N. Ferguson,et al.  Control of scrapie in the UK sheep population , 2008, Epidemiology and Infection.

[30]  R. Ward,et al.  Experimental infection studies of uk Culicoides species midges with bluetongue virus serotypes 8 and 9 , 2008, Veterinary Record.

[31]  A. Gerry,et al.  Seasonal Transmission of Bluetongue Virus by Culicoides sonorensis (Diptera: Ceratopogonidae) at a Southern California Dairy and Evaluation of Vectorial Capacity as a Predictor of Bluetongue Virus Transmission , 2001, Journal of medical entomology.

[32]  R. A. Nunamaker,et al.  Applications of dot-blot, ELISA, and immunoelectron microscopy to field detection of bluetongue virus in Culicoides variipennis sonorensis: an ecological perspective. , 1997, Journal of medical entomology.

[33]  S. Gubbins,et al.  An assessment of Culicoides surveillance techniques in northern Europe: have we underestimated a potential bluetongue virus vector? , 2008 .

[34]  G. Gerbier,et al.  Field observations during the Bluetongue serotype 8 epidemic in 2006. II. Morbidity and mortality rate, case fatality and clinical recovery in sheep and cattle in the Netherlands. , 2008, Preventive veterinary medicine.

[35]  F. Conraths,et al.  Bluetongue virus serotype 8 epidemic in North-Western Europe in 2006: preliminary findings , 2007 .

[36]  A. Tatem,et al.  Modelling the distributions of Culicoides bluetongue virus vectors in Sicily in relation to satellite‐derived climate variables , 2004, Medical and veterinary entomology.

[37]  James Truscott,et al.  Control of a highly pathogenic H5N1 avian influenza outbreak in the GB poultry flock , 2007, Proceedings of the Royal Society B: Biological Sciences.

[38]  P. Mellor,et al.  Rates of bluetongue virus transmission between Culicoides sonorensis and sheep , 2008, Medical and veterinary entomology.

[39]  Rob Deardon,et al.  Optimal reactive vaccination strategies for a foot-and-mouth outbreak in the UK , 2006, Nature.

[40]  G. Gerbier,et al.  Modelling local dispersal of bluetongue virus serotype 8 using random walk. , 2008, Preventive veterinary medicine.

[41]  S. Cornell,et al.  Dynamics of the 2001 UK Foot and Mouth Epidemic: Stochastic Dispersal in a Heterogeneous Landscape , 2001, Science.

[42]  C. Faes,et al.  Epidemiological analysis of the 2006 bluetongue virus serotype 8 epidemic in north-western Europe Role of human interventions , 2006 .

[43]  S. Gubbins A modelling framework to describe the spread of scrapie between sheep flocks in Great Britain. , 2005, Preventive veterinary medicine.

[44]  R Meiswinkel,et al.  Mapping the basic reproduction number (R₀) for vector-borne diseases: a case study on bluetongue virus. , 2009, Epidemics.

[45]  C. Witham,et al.  Bluetongue in the United Kingdom and northern Europe in 2007 and key issues for 2008 , 2008, Veterinary Record.

[46]  N. Ferguson,et al.  Transmission Parameters of the 2001 Foot and Mouth Epidemic in Great Britain , 2007, PloS one.

[47]  A. Gerry,et al.  Seasonal Abundance and Survivorship of Culicoides sonorensis (Diptera: Ceratopogonidae) at a Southern California Dairy, with Reference to Potential Bluetongue Virus Transmission and Persistence , 2000, Journal of medical entomology.

[48]  M. D. de Jong,et al.  Modelling the effectiveness and risks of vaccination strategies to control classical swine fever epidemics , 2009, Journal of The Royal Society Interface.

[49]  E. M. Nevill The use of cattle to protect sheep from bluetongue infection. , 1978, Journal of the South African Veterinary Association.

[50]  A. Tatem,et al.  Prediction of bluetongue vector distribution in Europe and north Africa using satellite imagery. , 2003, Veterinary microbiology.

[51]  P. Mellor,et al.  Effect of temperature on the transmission of orbiviruses by the biting midge, Culicoides sonorensis , 2002, Medical and veterinary entomology.

[52]  E. Greiner,et al.  The epidemiology of bluetongue. , 1994, Comparative immunology, microbiology and infectious diseases.

[53]  R. Christley,et al.  Epidemiological consequences of an incursion of highly pathogenic H5N1 avian influenza into the British poultry flock , 2008, Proceedings of the Royal Society B: Biological Sciences.

[54]  Christl A. Donnelly,et al.  Transmission intensity and impact of control policies on the foot and mouth epidemic in Great Britain , 2001, Nature.