The potential role of wild and feral animals as reservoirs of foot-and-mouth disease

We investigated the potential role of feral pigs and wild deer as FMD reservoirs with a susceptible-latent-infected-recovered geographic-automata model, using spatially referenced data from southern Texas, USA. An uncontrolled FMD outbreak initiated in feral pigs and in wild deer might infect up to 698 (90% prediction interval 181, 1387) and 1557 (823, 2118) cattle and affect an area of 166 km(2) (53, 306) and 455 km(2) (301, 588), respectively. The predicted spread of FMD virus infection was influenced by assumptions we made regarding the number of incursion sites and the number of neighborhood interactions between herds. Our approach explicitly incorporates the spatial relationships between domesticated and non-domesticated animal populations, providing a new framework to explore the impacts, costs, and strategies for the control of foreign animal diseases with a potential wildlife reservoir.     

The impact of seasonal variability in wildlife populations on the predicted spread of foot and mouth disease

Modeling potential disease spread in wildlife populations is important for predicting, responding to and recovering from a foreign animal disease incursion such as foot and mouth disease (FMD). We conducted a series of simulation experiments to determine how seasonal estimates of the spatial distribution of white-tailed deer impact the predicted magnitude and distribution of potential FMD outbreaks. Outbreaks were simulated in a study area comprising two distinct ecoregions in South Texas, USA, using a susceptible-latent-infectious-resistant geographic automata model (Sirca). Seasonal deer distributions were estimated by spatial autoregressive lag models and the normalized difference vegetation index. Significant (P < 0.0001) differences in both the median predicted number of deer infected and number of herds infected were found both between seasons and between ecoregions. Larger outbreaks occurred in winter within the higher deer-density ecoregion, whereas larger outbreaks occurred in summer and fall within the lower deer-density ecoregion. Results of this simulation study suggest that the outcome of an FMD incursion in a population of wildlife would depend on the density of the population infected and when during the year the incursion occurs. It is likely that such effects would be seen for FMD incursions in other regions and countries, and for other diseases, in cases in which a potential wildlife reservoir exists. Study findings indicate that the design of a mitigation strategy needs to take into account population and seasonal characteristics.     

Experimental infection of wild boar and domestic pigs with a foot and mouth disease virus strain detected in the southeast of Bulgaria in December of 2010

Foot and mouth disease (FMD) was detected in a wild boar in Southeastern Bulgaria in December 2010. The occurrence and spread of the disease in wild cloven-hoofed animals may pose an unexpected and significant threat to FMD virus (FMDV)-free areas within and outside the European Union. So far, only one well documented experimental infection with FMD in wild boar has been published. In order to obtain more epidemiologically relevant data regarding the disease in wild boar we conducted an experiment with the 2010 Bulgarian FMDV type O isolate. Two young wild boar were challenged while two domestic pigs and two additional wild boar served as contact controls. While the domestic pigs developed severe clinical signs of FMD, the wild boar showed relatively mild course of the disease. Viremia started in contact wild boar 2 days post exposure (DPE) and lasted until 6 DPE. The virus shedding lasted until 9 DPE. On 27 DPE, when the animals were slaughtered, viral RNA was detected in lymphoid tissues and oropharyngeal fluid but no virus could be isolated. Commercial ELISAs and virus neutralisation tests detected antibodies against FMDV on 8 or 6 DPE, respectively. The data of the present study will help to understand FMD in wild boar populations and can be used in models to evaluate the potential role of wild boar in FMD epidemiology.     

Simulating the spatial dynamics of foot and mouth disease outbreaks in feral pigs and livestock in Queensland, Australia, using a susceptible-infected-recovered cellular automata model

We describe an approach to modelling the spatio-temporal spread of foot and mouth disease through feral animal and unfenced livestock populations. We used a susceptible-infected-recovered model, implemented in a cellular automata framework, to assess the spread of FMD across two regions of Queensland, Australia. Following a sensitivity analysis on the infectious states, scenario analyses were conducted using feral pigs only as the susceptible population, and then with the addition of livestock, and initiated in the wet season and in the dry season. The results indicate that, depending on the season the outbreak is initiated, and without the implementation of control measures, an outbreak of Foot and Mouth Disease around Winton could continue unchecked, while an outbreak around Cape York may die out naturally. The approach explicitly incorporates the spatial relationships between the populations through which the disease spreads and provides a framework by which the spread of disease outbreaks can be explored through varying the model parameters. It highlights the emergence and importance of spatio-temporal patterns, something that previous modelling of FMD in feral animal and unfenced livestock populations has lacked.     

Modelling the spread of foot-and-mouth disease in Australia

Preparedness for an incursion of an exotic animal disease is of key importance to government, industry, producers and the Australian community. An important aspect of Australia's preparedness for a possible incursion of foot-and-mouth disease is investigation into the likely effectiveness and cost-efficiency of eradication strategies when applied to different regional outbreak scenarios. Disease modelling is a tool that can be used to study diseases such as foot-and-mouth disease to better understand potential disease spread and control under different conditions. The Australian Government Department of Agriculture, Fisheries and Forestry has been involved with epidemiologic simulation modelling for more than 10 years, and has developed a sophisticated spatial model for foot-and-mouth disease (AusSpread) that operates within a geographic information system framework. The model accommodates real farm boundary or point-location data, as well as synthesised data based on agricultural census and land use information. The model also allows for interactions between herds or flocks of different animal species and production type, and considers the role that such interactions are likely to play in the epidemiology of a regional outbreak of foot-and-mouth disease. The user can choose mitigations and eradication strategies from those that are currently described in Australia's veterinary emergency plan. The model also allows the user to evaluate the impact of constraints on the availability of resources for mitigations or eradication measures. Outputs include a range of maps and tabulated outbreak statistics describing the geographic extent of the outbreak and its duration, the numbers of affected, slaughtered, and, as relevant, vaccinated herds or flocks, and the cost of control and eradication. Cost-related outputs are based on budgets of the value of stock and the cost of mitigations, each of which can be varied by the user. These outputs are a valuable resource to assist with policy development and disease management.     

A review of foot-and-mouth disease with special consideration for the clinical and epidemiological factors relevant to predictive modelling of the disease

Modelling the epidemiology of foot-and-mouth disease (FMD) has been undertaken since the early 1970s. We review here clinical factors and modelling procedures that have been used in the past, differentiating between those that have proved to be more relevant in controlling FMD epidemics, and those that have showed less significance. During the 2001 UK FMD epidemic, many previously developed FMD models were available for consideration and use. Accurate epidemiological models can become useful tools for determining relevant control policies for different scenarios and, conversely, inaccurate models may become an abuse for disease control. Inaccuracy presents two opposing difficulties. Firstly, too much control (in terms of animal slaughter for 2001) would negatively impact the farming community for many subsequent years, whilst too little control would permit an epidemic to persist. Accuracy however, presents the optimal permutation of control measures that could be implemented for a given set of conditions, and is a prerequisite to boosting public confidence in the use of epidemiological models for future epidemics.     

Epidemiological simulation modeling and spatial analysis for foot-and-mouth disease control strategies: a comprehensive review

Foot-and-mouth disease (FMD) is one of the most serious transboundary, contagious viral diseases of cloven-hoofed livestock, because it can spread rapidly with high morbidity rates when introduced into disease-free herds or areas. Epidemiological simulation modeling can be developed to study the hypothetical spread of FMD and to evaluate potential disease control strategies that can be implemented to decrease the impact of an outbreak or to eradicate the virus from an area. Spatial analysis, a study of the distributions of events in space, can be applied to an area to investigate the spread of animal disease. Hypothetical FMD outbreaks can be spatially analyzed to evaluate the effect of the event under different control strategies. The main objective of this paper is to review FMD-related articles on FMD epidemiology, epidemiological simulation modeling and spatial analysis with the focus on disease control. This review will contribute to the development of models used to simulate FMD outbreaks under various control strategies, and to the application of spatial analysis to assess the outcome of FMD spread and its control.     

A point pattern model of the spread of foot-and-mouth disease

The spatial spread of foot-and-mouth disease (FMD) is influenced by several sources of spatial heterogeneity: heterogeneity of the exposure to the virus, heterogeneity of the animal density and heterogeneity of the networks formed by the contacts between farms. A discrete space model assuming that farms can be reduced to points is proposed to handle these different factors. The farm-to-farm process of transmission of the infection is studied using point-pattern methodology. Farm management, commercial exchanges, possible airborne transmission, etc. cannot be explicitly taken into account because of lack of data. These latter factors are introduced via surrogate variables such as herd size and distance between farms. The model is built on the calculation of an infectious potential for each farm.This method has been applied to the study of the 1967-1968 FMD epidemic in UK and allowed us to evaluate the spatial variation of the probability of infection during this epidemic. Maximum likelihood estimation has been conducted conditional on the absence of data concerning the farms which were not infected during the epidemic. Model parameters have then been tested using an approximated conditional-likelihood ratio test. In this case study, results and validation are limited by the lack of data, but this model can easily be extended to include other information such as the effect of wind direction and velocity on airborne spread of the virus or the complex interactions between the locations of farms and the herd size. It can also be applied to other diseases where point approximation is convenient. In the context of an increase of animal density in some areas, the model explicitly incorporates the density and known epidemiological characteristics (e.g. incubation period) in the calculation of the probability of FMD infection. Control measures such as vaccination or slaughter can be simply introduced, respectively, as a reduction of the susceptible population or as a reduction of the source of infection.     

Experimental evaluation of foot-and-mouth disease vaccines for emergency use in ruminants and pigs: a review

Changes to foot-and-mouth disease (FMD) control policies since 2001 mean that emergency vaccination must be considered more readily as a control measure in the future. Since field application of vaccine for emergency use has only rarely been applied, the effectiveness of single dose administration, as a control measure in an outbreak situation, is poorly understood. In this review we consider all the available experimental data from studies utilizing either experimental or readily available, commercially produced vaccines, in order to assess their likely effectiveness as an additional means of controlling FMD transmission and spread in an emergency. Overall it is concluded that such vaccines offer an additional and valuable means of FMD control for both ruminants and pigs. They are able to reduce clinical disease, sub-clinical infection and excretion and onward transmission of virus. However, to be most effective, vaccination should be rapidly applied to give maximum opportunity for immunity to develop. We also identify areas for future research and emphasize the importance of vaccine efficacy studies in providing data for models that can help to predict the efficacy of differing FMD control strategies.     

Identifying spatio-temporal patterns of transboundary disease spread: examples using avian influenza H5N1 outbreaks

Characterizing spatio-temporal patterns among epidemics in which the mechanism of spread is uncertain is important for generating disease spread hypotheses, which may in turn inform disease control and prevention strategies. Using a dataset representing three phases of highly pathogenic avian influenza H5N1 outbreaks in village poultry in Romania, 2005–2006, spatio-temporal patterns were characterized. We first fit a set of hierarchical Bayesian models that quantified changes in the spatio-temporal relative risk for each of the 23 affected counties. We then modeled spatial synchrony in each of the three epidemic phases using non-parametric covariance functions and Thin Plate Spline regression models. We found clear differences in the spatio-temporal patterns among the epidemic phases (local versus regional correlated processes), which may indicate differing spread mechanisms (for example wild bird versus human-mediated). Elucidating these patterns allowed us to postulate that a shift in the primary mechanism of disease spread may have taken place between the second and third phases of this epidemic. Information generated by such analyses could assist affected countries in determining the most appropriate control programs to implement, and to allocate appropriate resources to preventing contact between domestic poultry and wild birds versus enforcing bans on poultry movements and quarantine. The methods used in this study could be applied in many different situations to analyze transboundary disease data in which only location and time of occurrence data are reported.     

Foot-and-mouth disease: susceptibility of domestic poultry and free-living birds to infection and to disease--a review of the historical and current literature concerning the role of birds in spread of foot-and-mouth disease viruses

Ruminants and pigs are the dominant natural hosts of food-and-mouth disease (FMD) viruses. Approximately 70 additional mammalian species are found to be susceptible under natural or experimental conditions. Reptilia, amphibia, and fish are probably naturally resistant to infection. According to the reviewed literature, domestic birds (chickens, turkeys, guinea fowl, ducks and geese) have been experimentally infected with some strains of FMD viruses and may develop lesions suggestive of FMD such as vesicular lesions on the comb, wattles, eye lids, and feet. Since chickens are to some extent coprophagous, chickens get infected by ingestion of virus under conditions of natural exposure or their plumage gets contaminated in an infectious environment. Thus, domestic birds kept in free-run systems may serve as virus vectors for short distances. Free-living birds, especially starlings (Sturnus vulgaris), sea gulls (Larus canus), house-sparrows (Passer domesticus) have been successfully experimentally infected and developed vesicular lesions on the skin and mucosal membranes of the mouth. During epizootics of FMD the plumage of these free-living birds can be contaminated with FMD viruses and the virus is spread over long distances during migration periods in spring and autumn. Thus migrating birds may assume an active role in long distance dissemination of FMD viruses.     

Modeling the spread and control of foot-and-mouth disease in Pennsylvania following its discovery and options for control

In this paper, we simulate outbreaks of foot-and-mouth disease in the Commonwealth of Pennsylvania, USA - after the introduction of a state-wide movement ban - as they might unfold in the presence of mitigation strategies. We have adapted a model previously used to investigate FMD control policies in the UK to examine the potential for disease spread given an infection seeded in each county in Pennsylvania. The results are highly dependent upon the county of introduction and the spatial scale of transmission. Should the transmission kernel be identical to that for the UK, the epidemic impact is limited to fewer than 20 premises, regardless of the county of introduction. However, for wider kernels where infection can spread further, outbreaks seeded in or near the county with highest density of premises and animals result in large epidemics (>150 premises). Ring culling and vaccination reduce epidemic size, with the optimal radius of the rings being dependent upon the county of introduction. Should the kernel width exceed a given county-dependent threshold, ring culling is unable to control the epidemic. We find that a vaccinate-to-live policy is generally preferred to ring culling (in terms of reducing the overall number of premises culled), indicating that well-targeted control can dramatically reduce the risk of large scale outbreaks of foot-and-mouth disease occurring in Pennsylvania.     

Modelling foot-and-mouth disease: a comparison between the UK and Denmark

Whilst the UK 2001 FMD (foot-and-mouth disease) outbreak provides an extremely rich source of spatio-temporal epidemic data, it is not clear how the models and parameters from the UK can be translated to other scenarios. Here we consider how the model framework used to capture the UK epidemic can be applied to a hypothetical FMD outbreak in Denmark. Whilst pigs played a relatively minor role in the UK epidemic (being the infected animal on just 18 farms), they dominate the Danish livestock landscape. In addition, it is not clear whether transmission parameters from the UK will transfer to Denmark where farming practices may be significantly different. We therefore explore a large volume of high-dimensional parameter space, but seek to relate final epidemic size, risk of spread to Danish islands and potential success of control measures, to early indicators of epidemic dynamics. The results of this extensive modelling exercise therefore allow us to provide timely advice on control options based on the observed behaviours of the first few generations.     

Foot-and-mouth disease: a review of intranasal infection of cattle, sheep and pigs

In an outbreak of foot-and-mouth disease (FMD) it is important to identify animals at risk from airborne virus. Investigations have been carried out over the years to determine the dose required to infect cattle, sheep and pigs by the intranasal route. This paper reviews the results of investigations for animals which have been infected by instillation or spraying a virus suspension into the nostrils or by exposure to affected animals through a mask or by indirect contact. The lowest doses were found by use of a mask. With virus from affected pigs given through a mask, doses of 18 infectious units (IU) in cattle and 8 IU in sheep were found to cause infection and give rise to lesions. Overall, cattle required the least amount of virus followed by sheep. Pigs required a dose of 22 IU to cause infection and a dose of 125 IU to give rise to lesions. In many experiments pigs failed to become infected. With all three species the dose varied with the individual animal and the virus strain. For modelling previous outbreaks and in real time, a dose of 8 IU or 10 and 50% infectious doses (ID50) could be used where cattle and sheep were involved. Experience in the field, combined with the results from experiments involving natural infection, indicate that pigs are not readily infected by the intranasal route. However, for modelling purposes a dose of about 25 IU should be used with care. Investigations are needed to determine doses for virus strains currently in circulation around the world. In addition, the nature of the aerosol droplets needs to be analysed to determine how the respective amounts of infective and non-infective virus particles, host components and, in later emissions, the presence of antibody affect the survival in air and ability to infect the respiratory tract. Further work is also required to correlate laboratory and field findings through incorporation of the doses into modelling the virus concentration downwind in order that those responsible for controlling FMD are provided with the best available assessment of airborne spread. Finally, the doses found for infection by the intranasal route could be applied to other methods of spread where virus is inhaled to assess risk.     

Foot-and-mouth disease and its differential diagnoses

Foot-and-mouth disease (FMD) is a highly contagious viral disease of cloven-hoofed animals, which leads to the formation of vesicles, erosions und ulcerations in the mouth and hairless parts of the skin, in particular on the feet. Due to its dramatic economic consequences, FMD is considered to be one of the most important diseases of animals. There is a permanent risk of introduction of the virus into Europe due to travel and illegal importation of agricultural products. Cloven-hoofed animals (cattle, sheep, goats, pigs and related game animals) are the typical hosts of the FMD virus. However, some zoo and wild animals belonging to other taxonomical groups, such as giraffes, elephants and camels, are also susceptible. Stomatitis and infections of the feet in livestock occur quite frequently, and often the causes of these conditions remain obscure. Sometimes, a differentiation from FMD is not possible on the basis of clinical signs and gross lesions, necessitating further laboratory investigations. This applies in particular to cases caused by the agents of vesicular stomatitis (VS) and swine vesicular disease (SVD). Additionally, other infectious agents can cause stomatitis, e.g. the viruses of mucosal disease (MD), malignant catarrhal fever (MCF), rinderpest, peste des petits ruminants (PPR), papular stomatitis, orf, blue tongue (BT) and epizootic haemorrhagic disease (EHD). In sheep, a stomatitis of unclear etiology was described as "OMAGOD". Furthermore, bacteria, chemicals and mechanical trauma can cause stomatitis and pododermatitis.     

Representation of animal distributions in space: how geostatistical estimates impact simulation modeling of foot-and-mouth disease spread

Modeling potential disease spread in wildlife populations is important for predicting, responding to and recovering from a foreign animal disease incursion. To make spatial epidemic predictions, the target animal species of interest must first be represented in space. We conducted a series of simulation experiments to determine how estimates of the spatial distribution of white-tailed deer impact the predicted magnitude and distribution of foot-and-mouth disease (FMD) outbreaks. Outbreaks were simulated using a susceptible-infected-recovered geographic automata model. The study region was a 9-county area (24 000 km(2)) of southern Texas. Methods used for creating deer distributions included dasymetric mapping, kriging and remotely sensed image analysis. The magnitudes and distributions of the predicted outbreaks were evaluated by comparing the median number of deer infected and median area affected (km(2)), respectively. The methods were further evaluated for similar predictive power by comparing the model predicted outputs with unweighted pair group method with arithmetic mean (UPGMA) clustering. There were significant differences in the estimated number of deer in the study region, based on the geostatistical estimation procedure used (range: 385 939-768 493). There were also substantial differences in the predicted magnitude of the FMD outbreaks (range: 1 563-8 896) and land area affected (range: 56-447 km(2)) for the different estimated animal distributions. UPGMA clustering indicated there were two main groups of distributions, and one outlier. We recommend that one distribution from each of these two groups be used to model the range of possible outbreaks. Methods included in cluster 1 (such as county-level disaggregation) could be used in conjunction with any of the methods in cluster 2, which included kriging, NDVI split by ecoregion, or disaggregation at the regional level, to represent the variability in the model predicted outbreak distributions. How animal populations are represented needs to be considered in all spatial disease spread models.     

A dynamic, optimal disease control model for foot-and-mouth disease: I. Model description

A dynamic optimization model was developed and used to evaluate alternative foot-and-mouth disease (FMD) control strategies. The model chose daily control strategies of depopulation and vaccination that minimized total regional cost for the entire epidemic duration, given disease dynamics and resource constraints. The disease dynamics and the impacts of control strategies on these dynamics were characterized in a set of difference equations; effects of movement restrictions on the disease dynamics were also considered. The model was applied to a three-county region in the Central Valley of California; the epidemic relationships were parameterized and validated using the information obtained from an FMD simulation model developed for the same region. The optimization model enables more efficient searches for desirable control strategies by considering all strategies simultaneously, providing the simulation model with optimization results to direct it in generating detailed predictions of potential FMD outbreaks.     

Developments in diagnostic techniques for differentiating infection from vaccination in foot-and-mouth disease

Foot-and-mouth disease (FMD) is a highly contagious and economically significant disease of cattle, pigs, sheep, goats and wild ruminant species. The FMD virus genome encodes a unique polyprotein from which the different viral polypeptides are cleaved by viral proteases, including eight different non-structural proteins (NSPs). Both structural and non-structural antigens induce the production of antibodies in infected animals. In contrast, vaccinated animals which have not been exposed to replicating virus will develop antibodies only to the viral antigens in the inactivated material. Vaccination against FMD is a key element in the control of the disease in addition to slaughter and movement restrictions. However, countries that vaccinate in the event of an outbreak will have to re-establish their FMD free status to the satisfaction of their trading partners.Because currently available vaccines stimulate the production of antibodies indistinguishable from those produced by infected animals in response to live virus and because vaccinated animals can be infected and become carriers of FMD virus, efforts have been made to develop diagnostic test that can differentiate vaccinated animals from those that are convalescent and from those that have been vaccinated and become carriers following subsequent contact with live virus. Currently the detection of antibodies to non-structural protein's (NSPs) is the preferred diagnostic method to distinguish virus infected, carrier, animals from vaccinated animals. However this is currently only possible at the herd level because of the great variability in the initiation, specificity and duration of the immune response in individual animals to the NSPs shown in many studies. Considerable effort and attention is now being directed toward the development of new methods and techniques for the rapid and accurate detection of anti-NSP antibodies, harmonization and standardization of current diagnostic techniques, as well as the production of defined reagents.     

The 2010 foot-and-mouth disease epidemic in Japan

Foot-and-mouth disease (FMD) occurred recently for the first time in a decade in Japan. The index case was detected on a beef-breeding farm in Miyazaki Prefecture, Southern Japan, on April 20, 2010. After confirmation of this first case, control measures such as stamping out, movement restriction and disinfection were implemented. However, these strategies proved insufficient to prevent the spread of FMD and emergency vaccination was adopted. Up until the last outbreak on July 4, 2010, a total of 292 outbreaks had been confirmed, with about 290,000 animals having been culled. The epidemic occurred in an area with a high density of cattle and pigs, making disease control difficult. Invasion of the disease into a high-density area aided its rapid spread and led to difficulties in locating suitable burial sites. Epidemiological investigations indicated that the disease was introduced into Japan approximately one month before detection. This delay in initial detection is considered to have allowed an increased number of outbreaks in the early stage of the epidemic. Nevertheless, the epidemic was contained within a localized area in Miyazaki Prefecture and was eradicated within three months because of intensive control efforts including emergency vaccination. Although this epidemic devastated the livestock industry in Japan, many lessons can be learnt for the future prevention and control of infectious diseases in animals.     

A practitioner's primer on foot-and-mouth disease

Foot-and-mouth disease (FMD) is caused by an RNA virus of the genus Aphthovirus; 7 immunologically distinct serotypes of the virus have been identified. Susceptible species are mainly domestic and wild even-toed ungulates, such as cattle, sheep, goats, pigs, bison, and deer. All body fluids of infected animals can contain the virus and are considered infective. The primary mode of transmission is animal-to-animal transmission through inhalation or ingestion of aerosols containing the virus. The virus can also be spread mechanically by contaminated organic debris and fomites and can survive for 48 hours on human oral and nasal mucosa and be spread to uninfected animals in this manner. There is a rapid progression of clinical signs after an animal becomes infected, and the virus spreads rapidly throughout a herd. Clinical signs include excessive salivation; fever; vesicles and erosions of the oral and nasal mucosa, coronary band, interdigital area, and teats; lameness; sloughing of claws; reluctance to move; anorexia; mastitis; decreased milk production; and abortion or weak newborns. In mature animals, FMD has high morbidity and low mortality rates. Infected animals can become inapparent carriers of the virus.