Optimising risk-based surveillance for early detection of invasive plant pathogens.

Emerging infectious diseases (EIDs) of plants continue to devastate ecosystems and livelihoods worldwide. Effective management requires surveillance to detect epidemics at an early stage. However, despite the increasing use of risk-based surveillance programs in plant health, it remains unclear how best to target surveillance resources to achieve this. We combine a spatially explicit model of pathogen entry and spread with a statistical model of detection and use a stochastic optimisation routine to identify which arrangement of surveillance sites maximises the probability of detecting an invading epidemic. Our approach reveals that it is not always optimal to target the highest-risk sites and that the optimal strategy differs depending on not only patterns of pathogen entry and spread but also the choice of detection method. That is, we find that spatial correlation in risk can make it suboptimal to focus solely on the highest-risk sites, meaning that it is best to avoid 'putting all your eggs in one basket'. However, this depends on an interplay with other factors, such as the sensitivity of available detection methods. Using the economically important arboreal disease huanglongbing (HLB), we demonstrate how our approach leads to a significant performance gain and cost saving in comparison with conventional methods to targeted surveillance.

Eco-Epidemiological Uncertainties of Emerging Plant Diseases: The Challenge of Predicting Xylella fastidiosa Dynamics in Novel Environments.

In order to prevent and control the emergence of biosecurity threats such as vector-borne diseases of plants, it is vital to understand drivers of entry, establishment, and spatiotemporal spread, as well as the form, timing, and effectiveness of disease management strategies. An inherent challenge for policy in combatting emerging disease is the uncertainty associated with intervention planning in areas not yet affected, based on models and data from current outbreaks. Following the recent high-profile emergence of the bacterium Xylella fastidiosa in a number of European countries, we review the most pertinent epidemiological uncertainties concerning the dynamics of this bacterium in novel environments. To reduce the considerable ecological and socio-economic impacts of these outbreaks, eco-epidemiological research in a broader range of environmental conditions needs to be conducted and used to inform policy to enhance disease risk assessment, and support successful policy-making decisions. By characterizing infection pathways, we can highlight the uncertainties that surround our knowledge of this disease, drawing attention to how these are amplified when trying to predict and manage outbreaks in currently unaffected locations. To help guide future research and decision-making processes, we invited experts in different fields of plant pathology to identify data to prioritize when developing pest risk assessments. Our analysis revealed that epidemiological uncertainty is mainly driven by the large variety of hosts, vectors, and bacterial strains, leading to a range of different epidemiological characteristics further magnified by novel environmental conditions. These results offer new insights on how eco-epidemiological analyses can enhance understanding of plant disease spread and support management recommendations.[Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

A method of determining where to target surveillance efforts in heterogeneous epidemiological systems.

The spread of pathogens into new environments poses a considerable threat to human, animal, and plant health, and by extension, human and animal wellbeing, ecosystem function, and agricultural productivity, worldwide. Early detection through effective surveillance is a key strategy to reduce the risk of their establishment. Whilst it is well established that statistical and economic considerations are of vital importance when planning surveillance efforts, it is also important to consider epidemiological characteristics of the pathogen in question-including heterogeneities within the epidemiological system itself. One of the most pronounced realisations of this heterogeneity is seen in the case of vector-borne pathogens, which spread between 'hosts' and 'vectors'-with each group possessing distinct epidemiological characteristics. As a result, an important question when planning surveillance for emerging vector-borne pathogens is where to place sampling resources in order to detect the pathogen as early as possible. We answer this question by developing a statistical function which describes the probability distributions of the prevalences of infection at first detection in both hosts and vectors. We also show how this method can be adapted in order to maximise the probability of early detection of an emerging pathogen within imposed sample size and/or cost constraints, and demonstrate its application using two simple models of vector-borne citrus pathogens. Under the assumption of a linear cost function, we find that sampling costs are generally minimised when either hosts or vectors, but not both, are sampled.

Dog ownership, dog behaviour and transmission of Echinococcus spp. in the Alay Valley, southern Kyrgyzstan.

Echinococcosis is a re-emerging zoonotic disease in Kyrgyzstan, and the incidence of human infection has increased substantially since the collapse of the Soviet Union in 1991. Domestic dogs are hosts of Echinococcus spp. and play an important role in the transmission of these parasites. The demography, ecology and behaviour of dogs are therefore relevant in studying Echinococcus spp. transmission. Dog demographics, roles of dogs, dog movements and faecal environmental contamination were assessed in four rural communities in the Alay Valley, southern Kyrgyzstan. Arecoline purge data revealed for the first time that E. granulosus, E. canadensis and E. multilocularis were present in domestic dogs in the Alay Valley. Surveys revealed that many households had dogs and that dogs played various roles in the communities, as pets, guard dogs or sheep dogs. Almost all dogs were free to roam, and GPS data revealed that many moved outside their communities, thus being able to scavenge offal and consume rodents. Faecal environmental contamination was high, presenting a significant infection risk to the local communities.

Epidemiologically-based strategies for the detection of emerging plant pathogens.

Emerging pests and pathogens of plants are a major threat to natural and managed ecosystems worldwide. Whilst it is well accepted that surveillance activities are key to both the early detection of new incursions and the ability to identify pest-free areas, the performance of these activities must be evaluated to ensure they are fit for purpose. This requires consideration of the number of potential hosts inspected or tested as well as the epidemiology of the pathogen and the detection method used. In the case of plant pathogens, one particular concern is whether the visual inspection of plant hosts for signs of disease is able to detect the presence of these pathogens at low prevalences, given that it takes time for these symptoms to develop. One such pathogen is the ST53 strain of the vector-borne bacterial pathogen Xylella fastidiosa in olive hosts, which was first identified in southern Italy in 2013. Additionally, X. fastidiosa ST53 in olive has a rapid rate of spread, which could also have important implications for surveillance. In the current study, we evaluate how well visual surveillance would be expected to perform for this pathogen and investigate whether molecular testing of either tree hosts or insect vectors offer feasible alternatives. Our results identify the main constraints to each of these strategies and can be used to inform and improve both current and future surveillance activities.

Risk assessment of Xanthomonas citri pv. viticola for the EU.

Following a request from the European Commission, the EFSA Panel on Plant Health performed a risk assessment of Xanthomonas citri pv. viticola (Xcv). This pest causes bacterial canker of grapevine and is reported from Brazil and India. Two scenarios were considered: scenario A0 (current practice) and A2 (additional control measures). For the fresh grape import pathway, scenario A0 results in an order of magnitude of about one entry per 10 years (median; 90% uncertainty interval between ca. one entry per 18,000 years and ca. five entries per year). For the Vitis spp. plants for planting for research/breeding purposes import pathway, the risk of entry is several orders of magnitude smaller than the risk due to fresh grape import. This outcome is also obtained under scenario A2. The key entry uncertainties include import volume and transfer (for plants for planting), transfer and the disaggregation factor (for fresh grapes) and the limited availability of epidemiological data. The extent of the area favourable for Xcv establishment in the EU is uncertain, illustrating the limitations of climate suitability assessments when based on few data points and little epidemiological information. Nevertheless, the risk of Xcv establishment is only slightly lower than the risk of Xcv entry, i.e. no major establishment constraints are expected for most entries. Similarly, the risk of Xcv establishment is assessed as only slightly lower under current climate compared to the climate of 2041-2060. For grapevine growing areas in the EU with average yearly temperature above 17°C, the lag phase between establishment and spread is expected to be about 3 years (median; 90% range between ca. 6 months and ca. 6 years). Under the same scenario, the rate of spread by natural means is assessed to be ca. 300 m/year (median; 90% range between ca. 35 and ca. 800 m/year). The spread rate would be considerably higher considering movements of plants and cutting tools or machinery. The percentage of grapevine plants infected by Xcv in production sites as yearly average over a 30-year production cycle is estimated to be ca. 17% (median; 90% range between ca. 1.5% and ca. 46%) in table grapes and ca. 12% (median; 90% range between ca. 0.7% and ca. 37%) in wine grapes. Impacts have been reported to be severe in Brazil and India, but the estimates provided here show that there is considerable uncertainty about expected impacts in the EU.

Pest risk assessment of Amyelois transitella for the European Union.

Following a request from the European Commission, the EFSA Panel on Plant Health performed a pest risk assessment of Amyelois transitella (Lepidoptera: Pyralidae), the navel orangeworm, for the EU. The quantitative assessment considered two scenarios: (i) current practices and (ii) a requirement for chilled transport. The assessment focused on pathways of introduction, climatic conditions and cultivation of hosts allowing establishment, spread and impact. A. transitella is a common pest of almonds, pistachios and walnuts in California, which is the main source for these nuts imported into the EU. Based on size of the trade and infestation at origin, importation of walnuts and almonds from the USA was identified as the most important pathways for entry of A. transitella. Using expert knowledge elicitation (EKE) and pathway modelling, a median estimate of 2,630 infested nuts is expected to enter the EU each year over the next 5 years (90% certainty range (CR) from 338 to 26,000 infested nuts per year). However, due to estimated small likelihoods of transfer to a host, mating upon transfer and survival of founder populations, the number of populations that establish was estimated to be 0.000698 year-1 (median, 90% CR: 0.0000126-0.0364 year-1). Accordingly, the expected period between founding events is 1,430 years (median, 90% CR: 27.5-79,400 year). The likelihood of entry resulting in establishment is therefore considered very small. However, this estimate has high uncertainty, mainly concerning the processes of transfer of the insect to hosts and the establishment of founder populations by those that successfully transfer. Climate matching and CLIMEX modelling indicate that conditions are most suitable for establishment in the southern EU, especially around the Mediterranean basin. The median rate of natural spread was estimated to be 5.6 km/year (median, 90% CR 0.8-19.3 km/year), after an initial lag period of 3.1 year (mean, 90% CR 1.7-6.2 year) following the establishment of a founder population. If A. transitella did establish, estimated median yield losses in nuts were estimated to be in the order of 1-2% depending on the nut species and production system. A scenario requiring imports of nuts to be transported under chilled conditions was shown to provide potential to further reduce the likelihood of entry.

Quantifying the hidden costs of imperfect detection for early detection surveillance.

The global spread of pathogens poses an increasing threat to health, ecosystems and agriculture worldwide. As early detection of new incursions is key to effective control, new diagnostic tests that can detect pathogen presence shortly after initial infection hold great potential for detection of infection in individual hosts. However, these tests may be too expensive to be implemented at the sampling intensities required for early detection of a new epidemic at the population level. To evaluate the trade-off between earlier and/or more reliable detection and higher deployment costs, we need to consider the impacts of test performance, test cost and pathogen epidemiology. Regarding test performance, the period before new infections can be first detected and the probability of detecting them are of particular importance. We propose a generic framework that can be easily used to evaluate a variety of different detection methods and identify important characteristics of the pathogen and the detection method to consider when planning early detection surveillance. We demonstrate the application of our method using the plant pathogen Phytophthora ramorum in the UK, and find that visual inspec-tion for this pathogen is a more cost-effective strategy for early detection surveillance than an early detection diagnostic test. This article is part of the theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: epidemic forecasting and control'. This theme issue is linked with the earlier issue 'Modelling infectious disease outbreaks in humans, animals and plants: approaches and important themes'.

Update of the Scientific Opinion on the risks to plant health posed by Xylella fastidiosa in the EU territory.

EFSA was asked to update the 2015 EFSA risk assessment on Xylella fastidiosa for the territory of the EU. In particular, EFSA was asked to focus on potential establishment, short- and long-range spread, the length of the asymptomatic period, the impact of X. fastidiosa and an update on risk reduction options. EFSA was asked to take into account the different subspecies and Sequence Types of X. fastidiosa. This was attempted throughout the scientific opinion but several issues with data availability meant that this could only be partially achieved. Models for risk of establishment showed most of the EU territory may be potentially suitable for X. fastidiosa although southern EU is most at risk. Differences in estimated areas of potential establishment were evident among X. fastidiosa subspecies, particularly X. fastidiosa subsp. multiplex which demonstrated areas of potential establishment further north in the EU. The model of establishment could be used to develop targeted surveys by Member States. The asymptomatic period of X. fastidiosa varied significantly for different host and pathogen subspecies combinations, for example from a median of approximately 1 month in ornamental plants and up to 10 months in olive, for pauca. This variable and long asymptomatic period is a considerable limitation to successful detection and control, particularly where surveillance is based on visual inspection. Modelling suggested that local eradication (e.g. within orchards) is possible, providing sampling intensity is sufficient for early detection and effective control measures are implemented swiftly (e.g. within 30 days). Modelling of long-range spread (e.g. regional scale) demonstrated the important role of long-range dispersal and the need to better understand this. Reducing buffer zone width in both containment and eradication scenarios increased the area infected. Intensive surveillance for early detection, and consequent plant removal, of new outbreaks is crucial for both successful eradication and containment at the regional scale, in addition to effective vector control. The assessment of impacts indicated that almond and Citrus spp. were at lower impact on yield compared to olive. Although the lowest impact was estimated for grapevine, and the highest for olive, this was based on several assumptions including that the assessment considered only Philaenus spumarius as a vector. If other xylem-feeding insects act as vectors the impact could be different. Since the Scientific Opinion published in 2015, there are still no risk reduction options that can remove the bacterium from the plant in open field conditions. Short- and long-range spread modelling showed that an early detection and rapid application of phytosanitary measures, consisting among others of plant removal and vector control, are essential to prevent further spread of the pathogen to new areas. Further data collection will allow a reduction in uncertainty and facilitate more tailored and effective control given the intraspecific diversity of X. fastidiosa and wide host range.

Background matching in the brown shrimp Crangon crangon: adaptive camouflage and behavioural-plasticity.

A combination of burrowing behaviour and very efficient background matching makes the brown shrimp Crangon crangon almost invisible to potential predators and prey. This raises questions on how shrimp succeed in concealing themselves in the heterogeneous and dynamic estuarine habitats they inhabit and what type of environmental variables and behavioural factors affect their colour change abilities. Using a series of behavioural experiments, we show that the brown shrimp is capable of repeated fast colour adaptations (20% change in dark pigment cover within one hour) and that its background matching ability is mainly influenced by illumination and sediment colour. Novel insights are provided on the occurrence of non-adaptive (possibly stress) responses to background changes after long-time exposure to a constant background colour or during unfavourable conditions for burying. Shrimp showed high levels of intra- and inter-individual variation, demonstrating a complex balance between behavioural-plasticity and environmental adaptation. As such, the study of crustacean colour changes represents a valuable opportunity to investigate colour adaptations in dynamic habitats and can help us to identify the mayor environmental and behavioural factors influencing the evolution of animal background matching.

Seasonal pattern of Echinococcus re-infection in owned dogs in Tibetan communities of Sichuan, China and its implications for control.

BACKGROUND: Human cystic echinococcosis (CE) and alveolar echinococcosis (AE) are highly endemic in Tibetan communities of Sichuan Province. Previous research in the region indicated that domestic dog was the major source of human infection, and observations indicated that domestic dog could have more access to intermediate hosts of Echinococcus spp.: both domestic livestock (CE) viscera and small mammals (AE), in early winter and again in spring. We hypothesized that there would therefore be a significant increase in the risk of canine infection with Echinococcus spp. in these two seasons and conducted a reinfection study to investigate this further. METHODS: Faecal samples were collected from owned dogs in seven townships in Ganze Tibetan Autonomous Prefecture (Sichuan Province, China), and Echinococcus spp. infection status was determined using copro-antigen ELISA. Dogs were sampled in April (spring), July (early summer), September/October (autumn/early winter) and December (winter) in 2009; and in April (spring) 2010. Dogs were treated with praziquantel following each of the five sample collections to eliminate any tapeworms. Information on dog sex, age and body weight was also collected. The t-test, Fisher's exact test, Poisson regression and logistic regression were used to compare means and prevalences, and to identify factors associated with infection status. RESULTS: The proportion of female dogs was significantly lower than that of male dogs; female dogs had significantly higher (22.78 %) baseline copro-ELISA prevalence than males (11.88 %). Dog body weight, sex, age, county and previous infection status at any sampling point had no influence on the re-infection prevalence in general. Poisson regression did not found a significant influence on the re-infection prevalence due to different deworming/sampling time spans. Dogs exhibited significantly higher re-infection prevalences in spring and early summer of 2009 and in early winter between September/October and December of 2009, suggesting a higher infection pressure in these seasons comparing with other seasons. CONCLUSION: Following praziquantel treatment, dog body weight, sex, age, county, deworming time span and previous infection status at any sampling point had no influence on the re-infection prevalence in the region in general. The differences between re-infection prevalences were probably due to the seasonality in Echinoccocus spp. infection pressure in the region. Early winter, spring and early summer should be important seasons for optimal dog deworming intervention in these Tibetan communities.

Echinococcus granulosus: Epidemiology and state-of-the-art of diagnostics in animals.

Diagnosis and detection of Echinococcus granulosus (sensu lato) infection in animals is a prerequisite for epidemiological studies and surveillance of echinococcosis in endemic, re-emergent or emergent transmission zones. Advances in diagnostic approaches for definitive hosts and livestock, however, have not progressed equally over the last 20 years. Development of laboratory based diagnostics for canids using coproantigen ELISA and also coproPCR, have had a huge impact on epidemiological studies and more recently on surveillance during hydatid control programmes. In contrast, diagnosis of cystic echinococcosis (CE) in livestock still relies largely on conventional post-mortem inspection, despite a relatively low diagnostic sensitivity especially in early infections, as current serodiagnostics do not provide a sufficiently specific and sensitive practical pre-mortem alternative. As a result, testing of dog faecal samples by coproantigen ELISA, often combined with mass ultrasound screening programmes for human CE, has been the preferred approach for monitoring and surveillance in resource-poor endemic areas and during control schemes. In this article we review the current options and approaches for diagnosis of E. granulosus infection in definitive and animal intermediate hosts (including applications in non-domesticated species) and make conclusions and recommendations for further improvements in diagnosis for use in epidemiological studies and surveillance schemes.

Independent evaluation of a canine Echinococcosis Control Programme in Hobukesar County, Xinjiang, China.

The Xinjiang Uyghur Autonomous Region in northwest China is one of the world's most important foci for cystic echinococcosis. Domestic dogs are the main source for human infection, and previous studies in Xinjiang have found a canine Echinococcus spp. coproELISA prevalence of between 36% and 41%. In 2010 the Chinese National Echinococcosis Control Programme was implemented in Xinjiang, and includes regular dosing of domestic dogs with praziquantel. Six communities in Hobukesar County, northwest Xinjiang were assessed in relation to the impact of this control programme through dog necropsies, dog Echinococcus spp. coproantigen surveys based on Lot Quality Assurance Sampling (LQAS) and dog owner questionnaires. We found that 42.1% of necropsied dogs were infected with Echinococcus granulosus, and coproELISA prevalences were between 15% and 70% in the communities. Although approximately half of all dog owners reported dosing their dogs within the 12 months prior to sampling, coproELISA prevalence remained high. Regular praziquantel dosing of owned dogs in remote and semi-nomadic communities such as those in Hobukesar County is logistically very difficult and additional measures should be considered to reduce canine echinococcosis.

Farm level risk factors associated with severity of post-weaning multi-systemic wasting syndrome.

A cross-sectional study involving 147 pig farms across England was conducted in 2008-2009. Farm severity of post-weaning multi-systemic wasting syndrome (PMWS) was estimated through the use of an algorithm that combined data on post-weaning mortality, PMWS morbidity and proportion of porcine circovirus type 2 PCR positive pigs. Farms were classified as non/slightly, moderately or highly affected by PMWS. Data on potential PMWS risk factors were collected through interviews, on-farm assessment and serological sampling. Risk factors were identified using multivariable ordinal logistic regression and multivariable linear regression. Factors associated with increased PMWS severity were rearing growers indoors (OR=23.7), requiring a higher number of veterinarian visits per year (OR=9.6), having poorly isolated hospital pens (OR=6.4), buying replacement boars (OR=4.8) and seropositivity to Mycoplasma hyopneumoniae (OR=4.29); factors associated with decreased PMWS severity were low stocking density for growers (OR=0.07), adjusting diets at least three times between weaning and 14 weeks of age (OR=0.12), and requiring visitors to be at least 2 days pig free (OR=0.14). This study provides evidence of the association between environmental and management factors and PMWS severity, and suggests that other pathogens may be important co-factors for the disease. In addition, this study highlights the potential efficacy of biosecurity measures in the reduction/prevention of within-farm PMWS severity.

Prevalence and risk factors for swine influenza virus infection in the English pig population.

Infection of pigs with influenza viruses is a cause of considerable economic loss for pig farmers as well as a potential human health concern - as evidenced by the identification of genetic material derived from swine-adapted influenza viruses in an novel strain of H1N1 influenza virus in 2009. A study was conducted investigating the prevalence of influenza virus infection in a selection of 143 English pig herds between April 2008 and April 2009, which found evidence of recent virus circulation in over half of these herds (n=75). Farms which were sampled in the Summer months were found to have lower odds of recent virus circulation, as were farms containing pigs kept in straw yards. Additionally, farms containing pigs kept indoors and farms containing high numbers of finisher pigs per water space were found to have higher odds of recent virus circulation. It is hoped that further studies will expand on these findings, and may allow targeting of surveillance for influenza viruses in the English pig population.