Assessing the export trade risk of bluetongue virus serotypes 4 and 8 in France

Bluetongue (BT) causes an economic loss of $3 billion every year in the world. After two serious occurrences of BT (bluetongue virus [BTV] occurrence in 2006 and 2015), France has been controlling for decades, but it has not been eradicated. As the largest live cattle export market in the world, France is also one of the major exporters of breeding animals and genetic materials in the world. The biosafety of its exported cattle and products has always been a concern. The scenario tree quantitative model was used to analyze the risk of BTV release from French exported live cattle and bovine semen. The results showed that with the increase in vaccination coverage rates, the risk decreased. If the vaccine coverage is 0%, the areas with the highest average risk probability of BTV‐4 and BTV‐8 release from exported live cattle were Haute‐Savoie and Puy‐de‐Dôme, and the risk was 2.96 × 10–4 and 4.25 × 10–4, respectively. When the vaccine coverage was 90%, the risk probability of BTV‐4 and BTV‐8 release from exported live cattle was 2.96 × 10–5 and 4.24 × 10–5, respectively. The average probability of BTV‐8 release from bovine semen was 1.09 × 10–10. Sensitivity analysis showed that the probability of false negative polymerase chain reaction (PCR) test and the probability of BT infection in the bull breeding station had an impact on the model. The identification of high‐risk areas and the discovery of key control measures provide a reference for decision makers to assess the risk of French exports of live cattle and bovine semen.

[1]  V. Martín,et al.  Inhibition of the IFN Response by Bluetongue Virus: The Story So Far , 2021, Frontiers in Microbiology.

[2]  A. de Kruif,et al.  Transmission of Bluetongue Virus Serotype 8 by Artificial Insemination with Frozen–Thawed Semen from Naturally Infected Bulls , 2021, Viruses.

[3]  M. Beer,et al.  Putative Novel Serotypes ‘33’ and ‘35’ in Clinically Healthy Small Ruminants in Mongolia Expand the Group of Atypical BTV , 2020, Viruses.

[4]  J. Sánchez-Vizcaíno,et al.  Global emergence and evolutionary dynamics of bluetongue virus , 2020, Scientific Reports.

[5]  Y. Liao,et al.  Temporal and Spatial Distribution Trends of Human Brucellosis in Liaoning Province, China. , 2020, Transboundary and emerging diseases.

[6]  Joshua B. Singer,et al.  “Frozen evolution” of an RNA virus suggests accidental release as a potential cause of arbovirus re-emergence , 2020, PLoS biology.

[7]  J. Sánchez-Vizcaíno,et al.  Risk Assessment of African Swine Fever Virus Exposure to Sus scrofa in Japan Via Pork Products Brought in Air Passengers’ Luggage , 2020, Pathogens.

[8]  F. Conraths,et al.  Economic Impact of a Bluetongue Serotype 8 Epidemic in Germany , 2020, Frontiers in Veterinary Science.

[9]  S. Zientara,et al.  Clinical cases of Bluetongue serotype 8 in calves in France in the 2018-2019 winter. , 2019, Transboundary and emerging diseases.

[10]  H. Nauwynck,et al.  Failure to Remove Bluetongue Serotype 8 Virus (BTV-8) From in vitro Produced and in vivo Derived Bovine Embryos and Subsequent Transmission of BTV-8 to Recipient Cows After Embryo Transfer , 2019, Front. Vet. Sci..

[11]  P. V. van Rijn Prospects of Next-Generation Vaccines for Bluetongue , 2019, Front. Vet. Sci..

[12]  V. Rijn,et al.  Prospects of Next-Generation Vaccines for Bluetongue. , 2019 .

[13]  S. Cauchemez,et al.  A network-based approach to modelling bluetongue spread in France. , 2019, Preventive veterinary medicine.

[14]  V. Hénaux,et al.  Modeling Culicoides abundance in mainland France: implications for surveillance , 2019, Parasites & Vectors.

[15]  G. Caignard,et al.  Bluetongue Virus in France: An Illustration of the European and Mediterranean Context since the 2000s , 2019, Viruses.

[16]  S. Cauchemez,et al.  Using serological studies to reconstruct the history of bluetongue epidemic in French cattle under successive vaccination campaigns. , 2018, Epidemics.

[17]  D. Calavas,et al.  Estimation of French cattle herd immunity against bluetongue serotype 8 at the time of its re-emergence in 2015 , 2018, BMC Veterinary Research.

[18]  B. Durand,et al.  Serological status for BTV‐8 in French cattle prior to the 2015 re‐emergence , 2018, Transboundary and emerging diseases.

[19]  D. Pfeiffer,et al.  Quantitative Assessment of the Risk of Release of Foot‐and‐Mouth Disease Virus via Export of Bull Semen from Israel , 2017, Risk analysis : an official publication of the Society for Risk Analysis.

[20]  S. Nielsen Bluetongue: control, surveillance and safe movement of animals , 2017, EFSA journal. European Food Safety Authority.

[21]  A. Passantino,et al.  Pre-transport factors affecting the welfare of cattle during road transport for slaughter - a review. , 2016 .

[22]  E. Sergeant,et al.  Quantitative Risk Assessment for African Horse Sickness in Live Horses Exported from South Africa , 2016, PloS one.

[23]  S. Zientara,et al.  Epidemiological characteristics and clinicopathological features of bluetongue in sheep and cattle, during the 2014 BTV serotype 4 incursion in Greece , 2016, Tropical Animal Health and Production.

[24]  C. Fourichon,et al.  Quantification of the increase in the frequency of early calving associated with late exposure to bluetongue virus serotype 8 in dairy cows: implications for syndromic surveillance , 2016, Veterinary Research.

[25]  F. Zagmutt,et al.  Quantitative risk assessment of the likeihood of introducing porcine reproductive and respiratory syndrome virus into New Zealand through the importation of pig meat. , 2015, Revue scientifique et technique.

[26]  M. Palmarini Bluetongue: a rich history filled with many landmarks in virology……and more to be uncovered! , 2014, Virus research.

[27]  C. Ducrot,et al.  Did Vaccination Slow the Spread of Bluetongue in France? , 2014, PloS one.

[28]  C. Saegerman,et al.  Clinical pattern characterization of cattle naturally infected by BTV-8. , 2013, Transboundary and emerging diseases.

[29]  C. Saegerman,et al.  Viral RNA load in semen from bluetongue serotype 8-infected rams: relationship with sperm quality. , 2012, Veterinary journal.

[30]  S. Gubbins,et al.  Comparison of pre-emptive and reactive strategies to control an incursion of bluetongue virus serotype 1 to Great Britain by vaccination , 2012, Epidemiology and Infection.

[31]  C. Ducrot,et al.  Estimating front-wave velocity of infectious diseases: a simple, efficient method applied to bluetongue , 2011, Veterinary research.

[32]  A. Allepuz,et al.  Quantitative assessment of the probability of bluetongue virus transmission by bovine semen and effectiveness of preventive measures. , 2011, Theriogenology.

[33]  K. De Clercq,et al.  A duplex real-time RT-PCR for the detection of bluetongue virus in bovine semen. , 2010, Journal of virological methods.

[34]  S. Gubbins,et al.  Transplacental Transmission of Bluetongue Virus 8 in Cattle, UK , 2009, Emerging infectious diseases.

[35]  Anthony J. Wilson,et al.  Bluetongue in Europe: past, present and future , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[36]  Guy Hendrickx,et al.  Field observations during the bluetongue serotype 8 epidemic in 2006. I. Detection of first outbreaks and clinical signs in sheep and cattle in Belgium, France and the Netherlands. , 2008, Preventive veterinary medicine.

[37]  K. De Clercq,et al.  Transplacental infection and apparently immunotolerance induced by a wild-type bluetongue virus serotype 8 natural infection. , 2008, Transboundary and emerging diseases.

[38]  D. Berkvens,et al.  Evaluation of antibody-ELISA and real-time RT-PCR for the diagnosis and profiling of bluetongue virus serotype 8 during the epidemic in Belgium in 2006. , 2008, Veterinary microbiology.

[39]  F. Landeg Bluetongue outbreak in the UK , 2007, Veterinary Record.

[40]  N. Murray International trade and the spread of animal diseases: assessing the risks. , 2006, Veterinaria italiana.

[41]  B. Osburn,et al.  Impact of bluetongue virus infection on the international movement and trade of ruminants. , 2006, Journal of the American Veterinary Medical Association.

[42]  A. Giovannini,et al.  The Use of Risk Assessment to Decide the Control Strategy for Bluetongue in Italian Ruminant Populations , 2004, Risk analysis : an official publication of the Society for Risk Analysis.

[43]  L. Melville,et al.  Excretion of bluetongue virus in cattle semen: a feature of laboratory-adapted virus. , 2004, Veterinaria italiana.

[44]  N J MacLachlan,et al.  Duration of viraemia infectious to Culicoides sonorensis in bluetongue virus-infected cattle and sheep. , 2002, Veterinary microbiology.

[45]  Vose Dj Risk analysis in relation to the importation and exportation of animal products. , 1997 .

[46]  B. Osburn,et al.  The impact of bluetongue virus on reproduction. , 1994, Comparative immunology, microbiology and infectious diseases.

[47]  A. Gould,et al.  Relationships amongst bluetongue viruses revealed by comparisons of capsid and outer coat protein nucleotide sequences. , 1990, Virus research.

[48]  B. M. Gorman,et al.  Analysis of the roles of bluetongue virus outer capsid proteins VP2 and VP5 in determination of virus serotype. , 1989, Virology.

[49]  康贞花,et al.  The Status Quo and Improvement Plan of China's Export Food Safety Supervision System , 2019 .

[50]  M. Tichit,et al.  Does biotechnological innovation require organizational innovation? Learning from the cattle breeding industry in France , 2016 .

[51]  E. Voslářová,et al.  Comparison of mortality rates in different categories of pigs and cattle during transport for slaughter , 2007 .