New tools to prevent the endemism of bluetongue
PhD Thesis defense by Cecilia Aguilar Vega at the VISAVET Centre of the Complutense University of Madrid
May 9th, 2022
Bluetongue is a transboundary arboviral disease transmitted mainly by species of the genus Culicoides. It affects essentially ruminants and has a great socioeconomic and animal health impact in areas where is present. Hence, it is a notifiable disease for the World Organization for Animal Health (OIE). At the end of the 20th century, it was considered an exotic disease in Europe, however, since 1998 there has been an incessant introduction and subsequent circulation of different strains of the bluetongue virus (BTV), the etiological agent of the disease. Its importance for the livestock industry justifies the study of the disease and its epidemiology to prevent its endemism in certain areas of Europe and specifically in Spain.
Thus, the main objective of this thesis entitled “New tools to prevent the endemism of bluetongue”, is to develop and apply tools to improve active surveillance, control and eradication plans for bluetongue in Spain.
Objective 1 examined the possible introduction of a previously absent European strain of BTV‐ 3 in Sicily from Tunisia through the passive dispersal of potentially infected midges of the genus Culicoides. The ADS dispersion model was applied, after adapting some aerodynamic parameters of the midges, and its results were compared with those obtained by the HYSPLIT model. Three possible introduction days were identified, of which September 2 was more likely based on the results of both models. The results obtained in this objective support the applicability of the ADS model for retrospective studies and as a tool for the active surveillance of diseases transmitted by Culicoides spp. once validated.
In Objective 2, a risk model for the persistence of BTV‐1 in mainland Spain was generated using only factors related to hosts and vectors. We created maximum abundance maps at 1 km2 spatial resolution for the main BTV vectors in Spain (Culicoides imicola and Obsoletus and Pulicaris complexes), with data from the entomological surveillance program of the ʺBluetongue National Surveillance Program, Control and Eradication in Spainʺ and environmental variables related to vector ecology. Random forest was chosen as the best machine learning algorithm in terms of predictive power (Subobjective 2.1.). The endemic model was generated including BTV‐1 historical circulation from 2010 to 2017, vector abundance, and farm density of domestic ruminant species, with the spatial resolution of the epidemiological unit of the Spanish active surveillance program (Subobjective 2.2.). The model suggested that BTV‐1 had greater risk of persistence in central and southwestern regions of Spain, being the three most relevant variables the abundance of C. imicola and Obsoletus complex, as well as the density of goat farms.
Objective 3 focused on assessing the risk of BTV transmission in mainland Spain and the Balearic Islands based on the basic reproduction number (R0) using a two‐host, two‐vector approach. The extension and spatiotemporal resolution of the study (1 km2 and monthly) are very valuable for decision‐making at a national level. Firstly, monthly abundance maps of the two most important vectors in the transmission of BTV in Spain, according to the literature and the results of the
previous objective (C. imicola and the Obsoletus complex), were generated with a methodology very similar to that of the previous objective (Subobjective 3.1.). For the calculation of the R0 throughout the territory of study, we used Culicoides spp. abundance models, as well as livestock density and average air temperature. The risk of transmission was categorized as low, medium and high (Subobjective 3.2.). The results of this objective evidenced the seasonality of BTV risk transmission in Spanish areas where historically BTV has circulated. We were able to identify two clearly differentiated areas of medium‐high risk: one in the northern region (where the Obsoletus complex is more abundant) and another in the central‐southern region (where C. imicola is the predominant species). Likewise, a natural barrier of low transmission risk has been identified between northern and central‐southern areas at risk that may hamper BTV spread between them.
Objective 4 aimed to expand the knowledge of the Obsoletus complex composition using the partial sequencing of the cox1 gene in poorly studied areas of Spain, as well as the genetic diversity of Culicoides obsoletus sensu stricto including georeferenced sequences. Information about species composition of the Obsoletus complex in the field could be relevant for epidemiological modelling when specific aspects of vector capacity of each species are available. A single‐tube multiplex PCR assay was designed to differentiate Obsoletus complex sibling species C. obsoletus and C. scoticus without the need for sequencing, although we found limitations in terms of specificity with C. montanus. Most of the 117 individuals analyzed were identified as C. obsoletus ss, being the proportion of C. scoticus much lower and residual that of C. montanus. Within C. obsoletus ss, 23 haplotypes were identified, being the genetic diversity of the populations studied much higher in the north of mainland Spain. The populations of the Canary Islands had low genetic flow with the rest of the sites, having also identified little genetic diversity in each one.
The complexity of bluetongue in terms of the interaction of the virus, the vector and the host, as well as its dispersion, imposes the need to approach epidemiological studies of the disease with a multidisciplinary approach that is reflected in the works contained in this thesis. All these studies can contribute to generating more efficient surveillance, control and eradication programs in terms of human, material and economic resources.
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