Risk of introduction of lumpy skin disease in France by the import of vectors in animal trucks

Abstract

Background: The lumpy skin disease virus (LSDV) is a dsDNA virus belonging to the Poxviridae family and the Capripoxvirus genus. Lumpy skin diseases (LSD) is a highly contagious transboundary disease in cattle producing major economic losses. In 2014, the disease was first reported in the European Union (in Cyprus); it was then reported in 2015 (in Greece) and has spread through different Balkan countries in 2016. Indirect vector transmission is predominant at small distances, but transmission between distant herds and between countries usually occurs through movements of infected cattle or through vectors found mainly in animal trucks.

Methods and principal findings: In order to estimate the threat for France due to the introduction of vectors found in animal trucks (cattle or horses) from at-risk countries (Balkans and neighbours), a quantitative import risk analysis (QIRA) model was developed according to the international standard. Using stochastic QIRA modelling and combining experimental/field data and expert opinion, the yearly risk of LSDV being introduced by stable flies (Stomoxys calcitrans), that travel in trucks transporting animals was between 6 x 10-5 and 5.93 x 10-3 with a median value of 89.9 x 10-5; it was mainly due to the risk related to insects entering farms in France from vehicles transporting cattle from the at-risk area. The risk related to the transport of cattle going to slaughterhouses or the transport of horses was much lower (between 2 x 10-7 and 3.73 x 10-5 and between 5 x 10-10 and 3.95 x 10-8 for cattle and horses, respectively). The disinsectisation of trucks transporting live animals was important to reduce this risk.

Conclusion and significance: The development of a stochastic QIRA made it possible to quantify the risk of LSD being introduced in France through the import of vectors that travel in trucks transporting animals. This tool is of prime importance because the LSD situation in the Balkans is continuously changing. Indeed, this model can be updated to process new information on vectors and the changing health situation, in addition to new data from the TRAde Control and Expert System (TRACES, EU database). This model is easy to adapt to different countries and to other vectors and diseases.

Fig 1. Risk pathways of LSD introduction from the at-risk area into France.

In grey, the modality estimated in this study.

Fig 2. Reported and posterior predicted numbers of infected vectors [A] and Posterior probability of LSDV surviving in Stomoxys calcitrans [B].

[A] The blue dots refer to the experimental results reported by [13], and the boxplots refer to the distribution of model predictions using the estimated posterior distribution; [B] Time refers to the number of days after an infective blood meal. The solid black lines and the red dots show the 95% credible interval and the median of the posterior distribution.

Fig 3. Conceptual framework for the estimation of the risk of lumpy skin disease being imported into France through vectors.

P1 to P10 are probabilities defined in the section named “Probabilities considered in the model”; Circular markers: animals; Triangular markers: vectors; Solid lines: transmission route for animals; Dotted lines: transmission route for vector; Blank circles: herd/farm in the area at-risk; Shaded circle: herd/farm in France.

Fig 4. Distribution of probabilities that vectors inside trucks of animals (cattle or horses) transmit LSD to native animals and sensitivity analysis.

A, C, E, G, and I represent the probabilities; B, D, F, H and J represent the sensitivity analyses (Spearman rank correlation coefficients are presented in decreasing order of importance).