New strategies for the prevention and control of african swine fever
Lina Mur Gil defended the PhD Thesis at the Faculty of Veterinary Medicine of the Complutense University of Madrid
October 29th, 2014
African swine fever (ASF) is one of the most complex and important diseases of swine. As it is a mandatory notifiable disease, its presence implies important socio-economic consequences in affected countries. Nowadays, ASF is endemic in a lot of countries within the African continent, posing a permanent risk of spread to free countries in other continents. This fact was clearly demonstrated by the last two escapes of ASF virus (ASFV) into Europe (1960 and 2007), that still nowadays are causing problems both in Sardinia (affected since 1978) and East Europe (affected in 2007). The lack of control and continuous spread in East Europe, even reaching European Union (EU) countries, has raised the awareness on this disease, partially forgot during these last decades.
This PhD thesis entitled “Development of new strategies for the prevention and control of African swine fever” has the goal of developing and providing new methodologies and tools for improving prevention and surveillance systems, as well as control programs against ASF in Europe. The work herein developed is summarized in nine scientific articles published in SCI (Science Citation Index) journals. These publications contain risk assessment methodologies, risk factors studies, models for control in endemic areas, as well as new methodologies for ASF surveillance.
The first objective includes the evaluation of the epidemiological situation of ASF, including the description of the ASF epidemiological scenarios currently present, as well as the detailed evolution and spread of the disease in Eastern Europe during the first five years of the epidemic. In addition, the risk factors present in East Europe that could be involved in the rapid spread of ASF and difficult its control, were identified. These risk factors include the absence of a coordinated and funded national control program in the Russian Federation, the abundant presence of back-yard pigs and other production systems with low biosecurity standards, and the frequent practice of swill feeding in the area. Most of these factors are socio-cultural, so their change would result very difficult, and consequently, the probability of ASF become endemic in the area is very high. These studies updated the information available about ASF epidemiology, enhancing the risk associated to the current distribution of ASF, specifically for some EU countries.
Consequently, the second objective consisted on the development of risk assessment studies for estimating the location and magnitude of the risk for ASFV introduction into EU through two of the most important routes of introduction. Specifically, the risk derived from the imports of live pigs during the high risk period was analyzed by a quantitative stochastic model. This model revealed a low probability of ASFV introduction by this pathway into the EU (5.22*10-3, which corresponds approximately with one outbreak every 192 years). Therefore, this route is not a current priority for the surveillance and control programs of the EU. In contrast, the risk associated to transport routes was estimated by the use of a semi-quantitative model, revealing that this risk was mainly concentrated in Poland (4.13/5) and Lithuania (3.8/5). The returning trucks was the sub-pathway at higher risk (65% of the total risk), followed by the waste form international boats and, ultimately, by the waste from international planes.
In addition, a modular tool was developed for the integration and joint visualization of all the risk assessments studied, including not only the two pathways analyzed in this thesis, but also three other pathways evaluated within a European project, in which assessments we also collaborated. This tool allows the global visualization and analysis of the results, revealing that 48% of EU countries presented a relative high risk for some of the routes analyzed. Important differences were observed among the different routes; while in some of them the risk was concentrated in few countries (transport associated fomites), others affected to 4 or 5 countries (legal imports of pigs, wild boar movement or illegal imports). This tool and the results provided in it could be used by EU member states for the adaptation and update of their surveillance and prevention programs based on the current existing risk. This modular tool developed herein has been published as supplementary material in an open access journal, so it is freely available, and it can be used for estimating ASF risk into other regions or periods of time.
The third objective is focused on the study of risk factors that difficult ASF control in endemic situations. The first study, located in Sardinia, evaluated ASF evolution during the 35 years of presence in the island, and identified the critical points that could have favored the persistence of the disease in the island. The abundant presence of small farms with low or null biosecurity measures, the presence of free non-controlled pigs (illegal) and the high density of wild boar in the island, were the most important identified factors. A new methodology based on the combination of spread and statistics models was developed for the evaluation of risk factors’ influence in endemic areas, as Sardinia. Firstly, we employed a disease spread model to simulate ASF spread within the domestic compartment, that reveals a general low spread of the disease (1.7 outbreaks on average), mainly caused by local spread. The comparison of these results with the ASF outbreaks occurred in Sardinia from 2007 to 21013, revealed a direct correlation between the biosecurity and control measures of the holdings and the potential spread of ASF in Sardinia. In contrast, the development of four logistic regression models revealed that both , the presence of illegal pigs and the density of wild boars are significant correlated with ASF occurrence. In general, illegal pigs have a higher influence; however, when very high densities of wild boar are present, this factor is more important. All these results were employed for creating risk maps for ASF spread and occurrence that would allow identifying the high risk areas for each factor, and consequently the priority areas to act. The adaptation of control measures to the specific factors identified in each area would result in an improvement of the efficacy of the programs, and a potential reduction of ASF prevalence in the island.
In parallel, a retrospective study was performed in a specific region of Spain for evaluating the importance of wild boar in ASF epidemiology, and its capability for maintaining ASF in the environment. For that purpose, 158 wild boar samples collected from one of the regions of Spain previously endemic for ASF, where ASF was most difficult to eradicate due to the presence of extensive pig production, ticks and wild boar, were evaluated. All of the samples were negative, revealing the inability of wild boar for maintaining ASF without the implication of other external sources of contamination. The methodologies developed and employed in these studies could be used in other regions for identifying and evaluating the role of risk factors present in the area. The adaptation of control and eradication programs to these risk factors is essential for the final eradication of the disease.
The fourth and last objective aims to facilitate ASF surveillance by the adaptation of serological techniques for the detection of antibodies against ASF in oral fluid. This study demonstrated for the first time, the presence of ASF antibodies in oral fluid of infected animals and the possibility of detecting them by the adjustment of two serological techniques (ELISA and IPT) previously available for serum samples. These results suggest the possibility of using this sample for ASF serological surveillance for the detection of survivor and carrier animals. Conversely, the potential use of oral fluid for the diagnosis of ASF acute forms is unprovable, as with the early appearance of high fever and mortality, diseased animals don’t react to the rope and it is almost impossible to obtain the sample. However, for serological surveillance, this sample presents several advantages comparing with serum samples. Firstly, it does not require bleeding animals, benefits welfare and animal management, and importantly, it is a non-invasive method that could be used for surveillance of wild populations by the use of some inviting substances in a simple and rapid way.
Results and methodologies developed in this thesis are novel and important with a direct application for the development and update of surveillance programs in the EU, as they provide a risk categorization for each of the countries. The identification and evaluation of risk factors in endemic territories is a useful tool for the design of control strategies in affected territories. These developments, together with the potential application of new diagnostic techniques for the diagnosis of oral fluid samples, are expected to result in an improvement of prevention of ASF entrance into EU, and a more effective control in ASF affected territories.
