Predicting spread and effective control measures for African swine fever-Should we blame the boars?

An ongoing, continually spreading, outbreak of African swine fever (ASF), following its identification in Georgia in 2007, has resulted in 17 European and 12 Asian countries reporting cases by April 2020, with cases occurring in both wild boar and domestic pigs. Curtailing further spread of ASF requires understanding of the transmission pathways of the disease. ASF is self-sustaining in the wild boar population, and they have been implicated as one of the main drivers of transmission within Europe. We developed a spatially explicit model to estimate the risk of infection with ASF in wild boar and pigs due to natural movement of wild boar that is applicable across the whole of Europe. We demonstrate the model by using it to predict the probability that early cases of ASF in Poland were caused by wild boar dispersion. The risk of infection in 2015 is computed due to wild boar cases in Poland in 2014, compared against reported cases in 2015, and then the procedure is repeated for 2015-2016. We find that long- and medium-distance spread of ASF (i.e. >30 km) is unlikely to have occurred due to wild boar dispersal, due in part to the generally short distances wild boar will travel (<20 km on average). We also predict the relative success of different control strategies in 2015, if they were implemented in 2014. Results suggest that hunting of wild boar reduces the number of new cases, but a larger region is at risk of ASF compared with no control measure. Alternatively, introducing wild boar-proof fencing reduces the size of the region at risk in 2015, but not the total number of cases. Overall, our model suggests wild boar movement is only responsible for local transmission of disease; thus, other pathways are more dominant in medium- and long-distance spread of the disease.

Cross-Validation of Generic Risk Assessment Tools for Animal Disease Incursion Based on a Case Study for African Swine Fever.

In recent years, several generic risk assessment (RA) tools have been developed that can be applied to assess the incursion risk of multiple infectious animal diseases allowing for a rapid response to a variety of newly emerging or re-emerging diseases. Although these tools were originally developed for different purposes, they can be used to answer similar or even identical risk questions. To explore the opportunities for cross-validation, seven generic RA tools were used to assess the incursion risk of African swine fever (ASF) to the Netherlands and Finland for the 2017 situation and for two hypothetical scenarios in which ASF cases were reported in wild boar and/or domestic pigs in Germany. The generic tools ranged from qualitative risk assessment tools to stochastic spatial risk models but were all parameterized using the same global databases for disease occurrence and trade in live animals and animal products. A comparison of absolute results was not possible, because output parameters represented different endpoints, varied from qualitative probability levels to quantitative numbers, and were expressed in different units. Therefore, relative risks across countries and scenarios were calculated for each tool, for the three pathways most in common (trade in live animals, trade in animal products, and wild boar movements) and compared. For the 2017 situation, all tools evaluated the risk to the Netherlands to be higher than Finland for the live animal trade pathway, the risk to Finland the same or higher as the Netherlands for the wild boar pathway, while the tools were inconclusive on the animal products pathway. All tools agreed that the hypothetical presence of ASF in Germany increased the risk to the Netherlands, but not to Finland. The ultimate aim of generic RA tools is to provide risk-based evidence to support risk managers in making informed decisions to mitigate the incursion risk of infectious animal diseases. The case study illustrated that conclusions on the ASF risk were similar across the generic RA tools, despite differences observed in calculated risks. Hence, it was concluded that the cross-validation contributed to the credibility of their results.

The Risk of Infection by African Swine Fever Virus in European Swine Through Boar Movement and Legal Trade of Pigs and Pig Meat.

African swine fever (ASF) is currently spreading westwards throughout Europe and eastwards into China, with cases occurring in both wild boar and domestic pigs. A generic risk assessment framework is used to determine the probability of first infection with ASF virus (ASFV) at a fine spatial scale across European Union Member States. The framework aims to assist risk managers across Europe with their ASF surveillance and intervention activities. Performing the risk assessment at a fine spatial scale allows for hot-spot surveillance, which can aid risk managers by directing surveillance or intervention resources at those areas or pathways deemed most at risk, and hence enables prioritization of limited resources. We use 2018 cases of ASF to estimate prevalence of the disease in both wild boar and pig populations and compute the risk of initial infection for 2019 at a 100 km2 cell resolution via three potential pathways: legal trade in live pigs, natural movement of wild boar, and legal trade in pig meat products. We consider the number of pigs, boar and amount of pig meat entering our area of interest, the prevalence of the disease in the origin country, the probability of exposure of susceptible pigs or boar in the area of interest to introduced infected pigs, boar, or meat from an infected pig, and the probability of transmission to susceptible animals. We provide maps across Europe indicating regions at highest risk of initial infection. Results indicate that the risk of ASF in 2019 was predominantly focused on those regions which already had numerous cases in 2018 (Poland, Lithuania, Hungary, Romania, and Latvia). The riskiest pathway for ASFV transmission to pigs was the movement of wild boar for Eastern European countries and legal trade of pigs for Western European countries. New infections are more likely to occur in wild boar rather than pigs, for both the pig meat and wild boar movement pathways. Our results provide an opportunity to focus surveillance activities and thus increase our ability to detect ASF introductions earlier, a necessary requirement if we are to successfully control the spread of this devastating disease for the pig industry.

A generic framework for spatial quantitative risk assessments of infectious diseases: Lumpy skin disease case study.

The increase in availability of spatial data and the technological advances to handle such data allow for subsequent improvements in our ability to assess risk in a spatial setting. We provide a generic framework for quantitative risk assessments of disease introduction that capitalizes on these new data. It can be adopted across multiple spatial scales, for any pathogen, method of transmission or location. The framework incorporates the risk of initial infection in a previously uninfected location due to registered movement (e.g., trade) and unregistered movement (e.g., daily movements of wild animals). We discuss the steps of the framework and the data required to compute it. We then outline how this framework is applied for a single pathway using lumpy skin disease as a case study, a disease which had an outbreak in the Balkans in 2016. We calculate the risk of initial infection for the rest of Europe in 2016 due to trade. We perform the risk assessment on 3 spatial scales-countries, regions within countries and individual farms. We find that Croatia (assuming no vaccination occurred) has the highest mean probability of infection, with Italy, Hungary and Spain following. Including import detection of infected trade does reduce risk but this reduction is proportionally lower for countries with highest risk. The risk assessment results are consistent across the spatial scales, while in addition, at the finer spatial scales, it highlights specific areas or individual locations of countries on which to focus surveillance.

Application of a quantitative entry assessment model to compare the relative risk of incursion of zoonotic bat-borne viruses into European Union Member States.

This paper presents a quantitative assessment model for the risk of entry of zoonotic bat-borne viruses into the European Union (EU). The model considers four routes of introduction: human travel, legal trade of products, live animal imports and illegal import of bushmeat and was applied to five virus outbreak scenarios. Two scenarios were considered for Zaire ebolavirus (wEBOV, cEBOV) and other scenarios for Hendra virus, Marburg virus (MARV) and Middle East Respiratory Syndrome Coronavirus (MERS-CoV). The use of the same framework and generic data sources for all EU Member States (MS) allows for a relative comparison of the probability of virus introduction and of the importance of the routes of introduction among MSs. According to the model wEBOV posed the highest risk of an introduction event within the EU, followed by MARV and MERS-CoV. However, the main route of introduction differed, with wEBOV and MERS-CoV most likely through human travel and MARV through legal trade of foodstuffs. The relative risks to EU MSs as entry points also varied between outbreak scenarios, highlighting the heterogeneity in global trade and travel to the EU MSs. The model has the capability to allow for a continual updating of the risk estimate using new data as, and when, it becomes available. The model provides an horizon scanning tool for use when available data are limited and, therefore, the absolute risk estimates often have high uncertainty. Sensitivity analysis suggested virus prevalence in bats has a large influence on the results; a 90% reduction in prevalence reduced the risk of introduction considerably and resulted in the relative ranking of MARV falling below that for MERS-CoV, due to this parameter disproportionately affecting the risk of introduction from the trade route over human travel.

U.K. Foot and Mouth Disease: A Systemic Risk Assessment of Existing Controls.

This article details a systemic analysis of the controls in place and possible interventions available to further reduce the risk of a foot and mouth disease (FMD) outbreak in the United Kingdom. Using a research-based network analysis tool, we identify vulnerabilities within the multibarrier control system and their corresponding critical control points (CCPs). CCPs represent opportunities for active intervention that produce the greatest improvement to United Kingdom's resilience to future FMD outbreaks. Using an adapted 'features, events, and processes' (FEPs) methodology and network analysis, our results suggest that movements of animals and goods associated with legal activities significantly influence the system's behavior due to their higher frequency and ability to combine and create scenarios of exposure similar in origin to the U.K. FMD outbreaks of 1967/8 and 2001. The systemic risk assessment highlights areas outside of disease control that are relevant to disease spread. Further, it proves to be a powerful tool for demonstrating the need for implementing disease controls that have not previously been part of the system.

A Generic Quantitative Risk Assessment Framework for the Entry of Bat-Borne Zoonotic Viruses into the European Union.

Bat-borne viruses have been linked to a number of zoonotic diseases; in 2014 there have been human cases of Nipah virus (NiV) in Bangladesh and Ebola virus in West and Central Africa. Here we describe a model designed to provide initial quantitative predictions of the risk of entry of such viruses to European Union (EU) Member States (MSs) through four routes: human travel, legal trade (e.g. fruit and animal products), live animal movements and illegal importation of bushmeat. The model utilises available datasets to assess the movement via these routes between individual countries of the world and EU MSs. These data are combined with virus specific data to assess the relative risk of entry between EU MSs. As a case study, the model was parameterised for NiV. Scenario analyses showed that the selection of exporting countries with NiV and potentially contaminated trade products were essential to the accuracy of all model outputs. Uncertainty analyses of other model parameters identified that the model expected number of years to an introduction event within the EU was highly susceptible to the prevalence of NiV in bats. The relative rankings of the MSs and routes, however, were more robust. The UK, the Netherlands and Germany were consistently the most likely points of entry and the ranking of most MSs varied by no more than three places (maximum variation five places). Legal trade was consistently the most likely route of entry, only falling below human travel when the estimate of the prevalence of NiV in bats was particularly low. Any model-based calculation is dependent on the data available to feed into the model and there are distinct gaps in our knowledge, particularly in regard to various pathogen/virus as well as host/bat characteristics. However, the strengths of this model lie in the provision of relative comparisons of risk among routes and MSs. The potential for expansion of the model to include other routes and viruses and the possibility of rapid parameterisation demonstrates its potential for use in an outbreak situation.

A Quantitative Microbiological Risk Assessment for Salmonella in Pigs for the European Union.

A farm-to-consumption quantitative microbiological risk assessment (QMRA) for Salmonella in pigs in the European Union has been developed for the European Food Safety Authority. The primary aim of the QMRA was to assess the impact of hypothetical reductions of slaughter-pig prevalence and the impact of control measures on the risk of human Salmonella infection. A key consideration during the QMRA development was the characterization of variability between E.U. Member States (MSs), and therefore a generic MS model was developed that accounts for differences in pig production, slaughterhouse practices, and consumption patterns. To demonstrate the parameterization of the model, four case study MSs were selected that illustrate the variability in production of pork meat and products across MSs. For the case study MSs the average probability of illness was estimated to be between 1 in 100,000 and 1 in 10 million servings given consumption of one of the three product types considered (pork cuts, minced meat, and fermented ready-to-eat sausages). Further analyses of the farm-to-consumption QMRA suggest that the vast majority of human risk derives from infected pigs with a high concentration of Salmonella in their feces (≥10(4) CFU/g). Therefore, it is concluded that interventions should be focused on either decreasing the level of Salmonella in the feces of infected pigs, the introduction of a control step at the abattoir to reduce the transfer of feces to the exterior of the pig, or a control step to reduce the level of Salmonella on the carcass post-evisceration.

Assessing the Effectiveness of On-Farm and Abattoir Interventions in Reducing Pig Meat-Borne Salmonellosis within E.U. Member States.

As part of the evidence base for the development of national control plans for Salmonella spp. in pigs for E.U. Member States, a quantitative microbiological risk assessment was funded to support the scientific opinion required by the EC from the European Food Safety Authority. The main aim of the risk assessment was to assess the effectiveness of interventions implemented on-farm and at the abattoir in reducing human cases of pig meat-borne salmonellosis, and how the effects of these interventions may vary across E.U. Member States. Two case study Member States have been chosen to assess the effect of the interventions investigated. Reducing both breeding herd and slaughter pig prevalence were effective in achieving reductions in the number of expected human illnesses in both case study Member States. However, there is scarce evidence to suggest which specific on-farm interventions could achieve consistent reductions in either breeding herd or slaughter pig prevalence. Hypothetical reductions in feed contamination rates were important in reducing slaughter pig prevalence for the case study Member State where prevalence of infection was already low, but not for the high-prevalence case study. The most significant reductions were achieved by a 1- or 2-log decrease of Salmonella contamination of the carcass post-evisceration; a 1-log decrease in average contamination produced a 90% reduction in human illness. The intervention analyses suggest that abattoir intervention may be the most effective way to reduce human exposure to Salmonella spp. However, a combined farm/abattoir approach would likely have cumulative benefits. On-farm intervention is probably most effective at the breeding-herd level for high-prevalence Member States; once infection in the breeding herd has been reduced to a low enough level, then feed and biosecurity measures would become increasingly more effective.

Characterization of the Human Risk of Salmonellosis Related to Consumption of Pork Products in Different E.U. Countries Based on a QMRA.

In response to the European Food Safety Authority's wish to assess the reduction of human cases of salmonellosis by implementing control measures at different points in the farm-to-consumption chain for pork products, a quantitative microbiological risk assessment (QMRA) was developed. The model simulated the occurrence of Salmonella from the farm to consumption of pork cuts, minced meat, and fermented ready-to-eat sausage, respectively, and a dose-response model was used to estimate the probability of illness at consumption. The QMRA has a generic structure with a defined set of variables, whose values are changed according to the E.U. member state (MS) of interest. In this article we demonstrate the use of the QMRA in four MSs, representing different types of countries. The predicted probability of illness from the QMRA was between 1 in 100,000 and 1 in 10 million per serving across all three product types. Fermented ready-to-eat sausage imposed the highest probability of illness per serving in all countries, whereas the risks per serving of minced meat and pork chops were similar within each MS. For each of the products, the risk varied by a factor of 100 between the four MSs. The influence of lack of information for different variables was assessed by rerunning the model with alternative, more extreme, values. Out of the large number of uncertain variables, only a few of them have a strong influence on the probability of illness, in particular those describing the preparation at home and consumption.

A Farm Transmission Model for Salmonella in Pigs, Applicable to E.U. Member States.

The burden of Salmonella entering pig slaughterhouses across the European Union is considered a primary food safety concern. To assist E.U. member states with the development of national control plans, we have developed a farm transmission model applicable to all member states. It is an individual-based stochastic susceptible-infected model that takes into account four different sources of infection of pigs (sows, feed, external contaminants such as rodents, and new stock) and various management practices linked to Salmonella transmission/protection (housing, flooring, feed, all-in-all-out production). A novel development within the model is the assessment of dynamic shedding rates. The results of the model, parameterized for two case study member states (one high and one low prevalence) suggest that breeding herd prevalence is a strong indicator of slaughter pig prevalence. Until a member state's' breeding herd prevalence is brought below 10%, the sow will be the dominant source of infection to pigs raised for meat production; below this level of breeding herd prevalence, feed becomes the dominant force of infection.

Potential for introduction of bat-borne zoonotic viruses into the EU: a review.

Bat-borne viruses can pose a serious threat to human health, with examples including Nipah virus (NiV) in Bangladesh and Malaysia, and Marburg virus (MARV) in Africa. To date, significant human outbreaks of such viruses have not been reported in the European Union (EU). However, EU countries have strong historical links with many of the countries where NiV and MARV are present and a corresponding high volume of commercial trade and human travel, which poses a potential risk of introduction of these viruses into the EU. In assessing the risks of introduction of these bat-borne zoonotic viruses to the EU, it is important to consider the location and range of bat species known to be susceptible to infection, together with the virus prevalence, seasonality of viral pulses, duration of infection and titre of virus in different bat tissues. In this paper, we review the current scientific knowledge of all these factors, in relation to the introduction of NiV and MARV into the EU.

Qualitative release assessment to estimate the likelihood of henipavirus entering the United Kingdom.

The genus Henipavirus includes Hendra virus (HeV) and Nipah virus (NiV), for which fruit bats (particularly those of the genus Pteropus) are considered to be the wildlife reservoir. The recognition of henipaviruses occurring across a wider geographic and host range suggests the possibility of the virus entering the United Kingdom (UK). To estimate the likelihood of henipaviruses entering the UK, a qualitative release assessment was undertaken. To facilitate the release assessment, the world was divided into four zones according to location of outbreaks of henipaviruses, isolation of henipaviruses, proximity to other countries where incidents of henipaviruses have occurred and the distribution of Pteropus spp. fruit bats. From this release assessment, the key findings are that the importation of fruit from Zone 1 and 2 and bat bushmeat from Zone 1 each have a Low annual probability of release of henipaviruses into the UK. Similarly, the importation of bat meat from Zone 2, horses and companion animals from Zone 1 and people travelling from Zone 1 and entering the UK was estimated to pose a Very Low probability of release. The annual probability of release for all other release routes was assessed to be Negligible. It is recommended that the release assessment be periodically re-assessed to reflect changes in knowledge and circumstances over time.

Assessing the risks of West Nile virus-infected mosquitoes from transatlantic aircraft: implications for disease emergence in the United Kingdom.

The number of West Nile virus (WNV)-infected mosquitoes aboard aircraft from the United States that arrive in the United Kingdom each summer was determined using a quantitative risk assessment. In the worst-case scenario, when WNV levels in mosquitoes are high (at epidemic levels) the probability of at least one WNV-infected mosquito being introduced into the United Kingdom was predicted to be 0.99. During these periods, a mean of 5.2 infected mosquitoes were estimated to be aboard flights from the United States to the United Kingdom during May to October, with 90% certainty that the exact value lies between one and ten mosquitoes. Heathrow airport was predicted to receive the majority of the infected mosquitoes (72.1%). Spatial analysis revealed the region surrounding Heathrow satisfies the criteria for potential WNV exposure as both WNV-competent mosquitoes and susceptible wild bird species are present. This region is, therefore, recommended for targeted, risk-based surveillance of WNV-infected mosquitoes in addition to an increased awareness of the risks to horses, birds and humans.

Attribution of human VTEC O157 infection from meat products: a quantitative risk assessment approach.

To address the risk posed to human health by the consumption of VTEC O157 within contaminated pork, lamb, and beef products within Great Britain, a quantitative risk assessment model has been developed. This model aims to simulate the prevalence and amount of VTEC O157 in different meat products at consumption within a single model framework by adapting previously developed models. The model is stochastic in nature, enabling both variability (natural variation between animals, carcasses, products) and uncertainty (lack of knowledge) about the input parameters to be modeled. Based on the model assumptions and data, it is concluded that the prevalence of VTEC O157 in meat products (joints and mince) at consumption is low (i.e., <0.04%). Beef products, particularly beef burgers, present the highest estimated risk with an estimated eight out of 100,000 servings on average resulting in human infection with VTEC O157.

A mathematical model for the transmission of Salmonella Typhimurium within a grower-finisher pig herd in Great Britain.

In a study of pigs slaughtered at British abattoirs, approximately 23% carried Salmonella in their cecal (large intestine) contents. The most frequent serotype was Salmonella Typhimurium (STM), which was the second most common cause of human salmonellosis in Great Britain. A pig industry-monitoring program was developed to reduce Salmonella infection on British farms. The control of STM infection on the farm requires an understanding of STM transmission dynamics within the herd, and a mathematical model has been developed for an infected grower-finisher farm. The model estimates the probability of a random pig being infected with STM. There are three broad categories of STM infection in pigs: pigs that are infected but unable to transmit the infection (latent); pigs that are infectious, i.e., able to transmit the infection (shedders); and pigs that have stopped shedding but harbor STM in their internal organs (carriers). The model estimates that 21.0% (5th and 95th percentiles, 0.05 to 77.5%) of slaughter-age pigs on an infected farm are likely to be shedding STM. Although this range is wide, it is biologically plausible. Sensitivity analysis of the total number of infected pigs revealed that the most significant input parameters are the probability of effective contact between a specific infectious and susceptible pig and the duration of shedding. The model predicted that 11.5% of pigs would be shedding STM at slaughter age. This value is close to the estimate obtained from a British abattoir survey that 11. 1% of pigs carried STM in their ceca, indicating that the model has reasonable validity.

Antimicrobial resistance: a microbial risk assessment perspective.

The emergence of antimicrobial-resistant microorganisms in both humans and food animals is a growing concern. Debate has centred on links between antimicrobial use in the production of food animals and the emergence of resistant organisms in the human population. Consequently, microbial risk assessment (MRA) is being used to facilitate scientific investigations of the risks related to the food chain, including quantification of uncertainty and prioritization of control strategies. MRA is a scientific tool that can be used to evaluate the level of exposure and the subsequent risk to human health relating to a specific organism or particular type of resistance. This paper reviews the recent applications of MRA in the area of antimicrobial resistance, and in particular, it focuses on the methods, assumptions and data limitations. Since MRA outputs are dependent on the quality of data inputs used in their development, we aim to promote the generation of good quality data by describing the properties that data should ideally possess for MRA and by highlighting the benefit of data generation specifically for inclusion in MRAs.