Indirect transmission via a contaminated environment can occur for a number of pathogens, even those typically thought of as being directly transmitted, such as influenza virus, norovirus, bovine tuberculosis, or foot-and-mouth disease virus (FMDV). Indirect transmission facilitates spread from multiple sources beyond the infectious host, complicating the epidemiology and control of these diseases. This study carried out a series of transmission experiments to determine the dose-response relationship between environmental contamination and transmission of FMDV in cattle from measurements of viral shedding and rates of environmental contamination and survival. Seven out of ten indirect exposures resulted in successful transmission. The basic reproduction number for environmental transmission of FMDV in this experimental setting was estimated at 1.65, indicating that environmental transmission alone could sustain an outbreak. Importantly, detection of virus in the environment prior to the appearance of clinical signs in infected cattle and successful transmission from these environments highlights there is a risk of environmental transmission even before foot-and-mouth disease (FMD) is clinically apparent in cattle. Estimated viral decay rates suggest that FMDV remained viable in this environment for up to 14 days, emphasizing the requirement for stringent biosecurity procedures following outbreaks of FMD and the design of control measures that reflect the biology of a pathogen. IMPORTANCE Effective control of a disease relies on comprehensive understanding of how transmission occurs, in order to design and apply effective control measures. Foot-and-mouth disease virus (FMDV) is primarily spread by direct contact between infected and naive individuals, although the high levels of virus shed by infected animals mean that virus can also be spread through contact with contaminated environments. Using a series of transmission experiments, we demonstrate that environmental transmission alone would be sufficient to sustain an outbreak. Key observations include that a risk of transmission exists before clinical signs of foot-and-mouth disease (FMD) are apparent in cattle and that survival of virus in the environment extends the transmission risk period. This study highlights the role a contaminated environment can play in the transmission of FMDV and presents approaches that can also be applied to study the transmission of other pathogens that are able to survive in the environment.
HighlightsFMDV A/ASIA/G-VII lineage has recently spread beyond the Indian sub-continent.Study evaluated the performance of a high potency polyvalent vaccine in cattle.A new vaccine strain should be developed which is tailored to the A/ASIA/G-VII lineage.
Prompt confirmation and diagnosis of disease are key factors in controlling outbreaks. The development of sampling techniques to detect FMDV RNA from the environment will extend the tool kit available for the surveillance of this pathogen. The methods presented in this article broaden surveillance opportunities using accessible techniques. Pairing these methods with existing and novel diagnostic tests will improve the capability for rapid detection of outbreaks and implementation of timely interventions to control outbreaks. In areas of endemicity, these methods can be implemented to extend surveillance beyond the investigation of clinical cases, providing additional data for the assessment of virus circulation in specific areas.
Foot-and-mouth disease (FMD) can cause large disruptive epidemics in livestock. Current eradication measures rely on the rapid clinical detection and removal of infected herds. Here, we evaluated the potential for preclinical diagnosis during reactive surveillance to reduce the risk of between-farm transmission. We used data from transmission experiments in cattle where both samples from individual animals, such as blood, probang samples, and saliva and nasal swabs, and herd-level samples, such as air samples, were taken daily during the course of infection. The sensitivity of each of these sample types for the detection of infected cattle during different phases of the early infection period was quantified. The results were incorporated into a mathematical model for FMD, in a cattle herd, to evaluate the impact of the early detection and culling of an infected herd on the infectious output. The latter was expressed as the between-herd reproduction ratio, Rh, where an effective surveillance approach would lead to a reduction in the Rh value to <1. Applying weekly surveillance, clinical inspection alone was found to be ineffective at blocking transmission. This was in contrast to the impact of weekly random sampling (i.e., using saliva swabs) of at least 10 animals per farm or daily air sampling (housed cattle), both of which were shown to reduce the Rh to <1. In conclusion, preclinical detection during outbreaks has the potential to allow earlier culling of infected herds and thereby reduce transmission and aid the control of epidemics.
The movements of undetected infected animals can facilitate long-distance pathogen spread, making control and eradication difficult by (re)infecting disease-free populations. Characterising movement patterns is essential in understanding pathogen spread and how potential interventions, particularly animal movement restrictions, could help as a control mechanism. In Northern Ireland (NI), cattle movements are important contributors to a significant portion of agricultural trade. They can be disrupted due to statutory interventions, for example, during bovine tuberculosis (bTB) control. Identifying populations at risk of becoming infected would allow for improved resource allocation. This could be through targeting herds with an above-average risk of becoming infected or spreading (amplifying) infection, and restricting their movement to manage future outbreaks. In this study, cattle movements were investigated using social network analysis (SNA) at the monthly temporal scale across NI during 2010-2015. Targeted and random herd restrictions were compared and their impact on the structure and connectivity of the networks' was assessed (e.g. connected component subgraphs). This work was contextualised in relation to bTB, the most persistent infectious disease currently impacting agriculture in NI, where reduced connectivity would represent potential reduced vulnerability from infection introduction. There was seasonal variation in network size and level of connectivity with spring and autumn being the largest and most connected due to common farming practices in NI. Across the study period, there was limited inter-annual variation in global network metrics. On average there were 6.28 movements between each pair of nodes each month, low reciprocity (mean of 0.155) and the networks were moderately accessible with an average path length of 4.28. Movements were not confined to within each disease management area but frequently occurred between these areas (mean assortativity of-0.0731) and herds with high degree interacted with herds of low degree (mean assortativity of-0.351). The Giant Weakly Connected Component (GWCC) spanned most of the networks (between 75% and 100% of nodes); however the Giant Strongly Connected Component (GSCC) included, at most, 23% of the network. There was heterogeneous contributions across NI with little participation in the GSCC from some disease management areas, and the GSCC was comprised predominantly of 'beef breeders', 'beef rearers', and 'other/mixed' type herds. Targeted restrictions were more effective at fragmenting the network than randomly restricting movements when 25% of nodes or more were removed. Cattle networks in NI are extremely interconnected and robust to movement restrictions, suggesting potential vulnerability to movementfacilitated pathogen spread, such as bTB.
Highlights Environmental and aerosol sampling can provide non-invasive methods of detection to supplement surveillance for FMD. The swab sampling methods tested are efficient at recovering FMDV from a range of surfaces likely to be found on a farm. The Coriolis micro air sampler was able to detect three serotypes of FMDV in aerosol samples.
The primary transmission route for foot-and-mouth disease (FMD), a contagious viral disease of cloven-hoofed animals, is by direct contact with infected animals. Yet indirect methods of transmission, such as via the airborne route, have been shown to play an important role in the spread of the disease. Airborne transmission of FMD is referred to as a low probability- high consequence event as a specific set of factors need to coincide to facilitate airborne spread. When conditions are favourable, airborne virus may spread rapidly and cause disease beyond the imposed quarantine zones, thus complicating control measures. Therefore, it is important to understand the nature of foot-and-mouth disease virus (FMDV) within aerosols; how aerosols are generated, viral load, how far aerosols could travel and survive under different conditions. Various studies have investigated emissions from infected animals under laboratory conditions, while others have incorporated experimental data in mathematical models to predict and trace outbreaks of FMD. However, much of the existing literature focussing on FMDV in aerosols describe work which was undertaken over 40 years ago. The aim of this review is to revisit existing knowledge and investigate how modern instrumentation and modelling approaches can improve our understanding of airborne transmission of FMD.
To control an outbreak of an infectious disease it is essential to understand the different routes of transmission and how they contribute to the overall spread of the pathogen. With this information, policy makers can choose the most efficient methods of detection and control during an outbreak. Here we demonstrate a method for assessing the contribution of different routes of transmission using approximate Bayesian computation with sequential Monte Carlo sampling (ABC-SMC). We apply this to infer parameters of an individual based model of within-herd transmission of foot-and-mouth disease virus (FMDV), incorporating transmission through direct contact and via environmental contamination. Additionally, we use ABC-SMC for model selection to assess the plausibility of either transmission route alone being responsible for all infections. We show that direct transmission likely contributes the majority of infections during an outbreak of FMD but there is an accumulation of environmental contamination that can cause infections within a farm and also have the potential to spread between farms via fomites.
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