Risk assessment of vector-borne diseases for public health governance.

OBJECTIVES: In the context of public health, risk governance (or risk analysis) is a framework for the assessment and subsequent management and/or control of the danger posed by an identified disease threat. Generic frameworks in which to carry out risk assessment have been developed by various agencies. These include monitoring, data collection, statistical analysis and dissemination. Due to the inherent complexity of disease systems, however, the generic approach must be modified for individual, disease-specific risk assessment frameworks. STUDY DESIGN: The analysis was based on the review of the current risk assessments of vector-borne diseases adopted by the main Public Health organisations (OIE, WHO, ECDC, FAO, CDC etc…). METHODS: Literature, legislation and statistical assessment of the risk analysis frameworks. RESULTS: This review outlines the need for the development of a general public health risk assessment method for vector-borne diseases, in order to guarantee that sufficient information is gathered to apply robust models of risk assessment. Stochastic (especially spatial) methods, often in Bayesian frameworks are now gaining prominence in standard risk assessment procedures because of their ability to assess accurately model uncertainties. CONCLUSIONS: Risk assessment needs to be addressed quantitatively wherever possible, and submitted with its quality assessment in order to enable successful public health measures to be adopted. In terms of current practice, often a series of different models and analyses are applied to the same problem, with results and outcomes that are difficult to compare because of the unknown model and data uncertainties. Therefore, the risk assessment areas in need of further research are identified in this article.

Predictive modelling of adult emergence in a polyphagous Eucolaspis (Chrysomelidae: Eumolpinae) leaf beetle.

Eucolaspis sp. "Hawke's Bay" (Chrysomelidae: Eumolpinae) is a pest that inflicts huge economic loss in many organic apple (Malus domestica Borkh.) orchards in New Zealand. The timing of control methods for this pest has been shown to be crucial for success. To aid in planning control programs, we studied threshold temperature and degree-days required for the development of Eucolaspis sp. "Hawke's Bay" pupae and modeled adult emergence in the field. Pupal development was observed at three constant temperatures. Pupae required 237.0 +/- 21.67 degree-days above lower threshold temperature of 4.7 degrees C +/- 0.89 degrees C to develop into adults. The emergence of adults was modeled with these thermal values and the model was tested for accuracy with field data. The model performed well with a precision of +/- 4 d. The proposed phenology model has wide applicability in monitoring and planning pest control measures.

Collection of Culicoides (Diptera: Ceratopogonidae) using CO2 and enantiomers of 1-octen-3-ol in the United Kingdom.

The host kairomones carbon dioxide (CO2) and 1-octen-3-ol elicit a host seeking response in a wide range of haematophagous Diptera. This study investigates the response of Culicoides biting midges (Diptera: Ceratopogonidae) to these cues using field-based experiments at two sites in the United Kingdom with very different species complements. Traps used for surveillance (miniature CDC model 512) and control (Mosquito Magnet Pro) were modified to release ratios of (R)- and (S)-1-octen-3-ol enantiomers in combination with CO2 and, in the case of the latter trap type, a thermal cue. Abundance and species diversity were then compared between these treatments and against collections made using a trap with a CO2 lure only, in a Latin square design. In both habitats, results demonstrated that semiochemical lures containing a high proportion of the (R)-enantiomer consistently attracted a greater abundance of host-seeking Culicoides females than any other treatment. Culicoides collected using an optimal stimulus of 500 ml/min CO2 combined with 4.1 mg/h (R)-1-octen-3-ol were then compared with those collected on sheep through the use of a drop trap. While preliminary in nature, this trial indicated Culicoides species complements are similar between collections made using the drop trap in comparison to the semiochemical-baited CDC trap, and that there are advantages in using (R)-1-octen-3-ol.

Mapping the basic reproduction number (R0) for vector-borne diseases: a case study on bluetongue virus.

Geographical maps indicating the value of the basic reproduction number, R0, can be used to identify areas of higher risk for an outbreak after an introduction. We develop a methodology to create R0 maps for vector-borne diseases, using bluetongue virus as a case study. This method provides a tool for gauging the extent of environmental effects on disease emergence. The method involves integrating vector-abundance data with statistical approaches to predict abundance from satellite imagery and with the biologically mechanistic modelling that underlies R0. We illustrate the method with three applications for bluetongue virus in the Netherlands: 1) a simple R0 map for the situation in September 2006, 2) species-specific R0 maps based on satellite-data derived predictions, and 3) monthly R0 maps throughout the year. These applications ought to be considered as a proof-of-principle and illustrations of the methods described, rather than as ready-to-use risk maps. Altogether, this is a first step towards an integrative method to predict risk of establishment of diseases based on mathematical modelling combined with a geographic information system that may comprise climatic variables, landscape features, land use, and other relevant factors determining the risk of establishment for bluetongue as well as of other emerging vector-borne diseases.

Invasion of bluetongue and other orbivirus infections into Europe: the role of biological and climatic processes.

The invasion of multiple strains of the midge-borne bluetongue virus into southern Europe since the late 1990s provides a rare example of a clear impact of climate change on a vector-borne disease. However, the subsequent dramatic continent-wide spread and burden of this disease has depended largely on altered biotic interactions with vector and host communities in newly invaded areas. Transmission by Palearctic vectors has facilitated the establishment of the disease in cooler and wetter areas of both northern and southern Europe. This paper discusses the important biological and climatic processes involved in these invasions, and the lessons that must be drawn for effective risk management of bluetongue and other midge-borne viruses in Europe.

Models for vectors and vector-borne diseases.

The development of models for species' distributions is briefly reviewed, concentrating on logistic regression and discriminant analytical methods. Improvements in each type of modelling approach have led to increasingly accurate model predictions. This review addresses several key issues that now confront those wishing to choose the "right" sort of model for their own application. One major issue is the number of predictor variables to retain in the final model. Another is the problem of sparse datasets, or of data reported to administrative levels only, not to points. A third is the incorporation of spatial co-variance and auto-covariance in the modelling process. It is suggested that many of these problems can be resolved by adopting an information-theoretic approach whereby a group of reasonable potential models is specified in advance, and the "best" candidate model is selected among them. This approach of model selection and multi-model inference, using various derivatives of the Kullback-Leibler information or distance statistic, puts the biologist, with her or his insight, back in charge of the modelling process that is usually the domain of statisticians. Models are penalized when they contain too many variables; careful specification of the right set of candidate models may also be used to identify the importance of each predictor variable individually; and finally the degree to which the current "best" model improves on all the other models in the candidate set may be quantified. The ability definitely to exclude some models from the realm of all possible models appropriate for any particular distribution problem may be as important as the ability to identify the best current model.

Global environmental data for mapping infectious disease distribution.

This contribution documents the satellite data archives, data processing methods and temporal Fourier analysis (TFA) techniques used to create the remotely sensed datasets on the DVD distributed with this volume. The aim is to provide a detailed reference guide to the genesis of the data, rather than a standard review. These remotely sensed data cover the entire globe at either 1 x 1 or 8 x 8 km spatial resolution. We briefly evaluate the relationships between the 1 x 1 and 8 x 8 km global TFA products to explore their inter-compatibility. The 8 x 8 km TFA surfaces are used in the mapping procedures detailed in the subsequent disease mapping reviews, since the 1 x 1 km products have been validated less widely. Details are also provided on additional, current and planned sensors that should be able to provide continuity with these environmental variable surfaces, as well as other sources of global data that may be used for mapping infectious disease.

The global distribution of yellow fever and dengue.

Yellow fever has been subjected to partial control for decades, but there are signs that case numbers are now increasing globally, with the risk of local epidemic outbreaks. Dengue case numbers have also increased dramatically during the past 40 years and different serotypes have invaded new geographical areas. Despite the temporal changes in these closely related diseases, and their enormous public health impact, few attempts have been made to collect a comprehensive dataset of their spatial and temporal distributions. For this review, records of the occurrence of both diseases during the 20th century have been collected together and are used to define their climatic limits using remotely sensed satellite data within a discriminant analytical model framework. The resulting risk maps for these two diseases identify their different environmental requirements, and throw some light on their potential for co-occurrence in Africa and South East Asia.

Tick-borne disease systems: mapping geographic and phylogenetic space.

Evidence is presented that the evolution of the tick-borne flaviviruses is driven by biotic factors, principally the exploitation of new hosts as transmission routes. Because vector-borne diseases are limited by climatic conditions, however, abiotic factors have the potential to direct and constrain the evolutionary pathways. This idea is explored by testing the hypothesis that closely related viruses occupy more similar eco-climatic spaces than do more distantly related viruses. A statistical comparison of the conventional phylogenetic tree derived from molecular distances and a novel phenetic tree derived from distances between the climatic spaces within which each virus circulates, indicates that these trees match each other more closely than would be expected at random. This suggests that these viruses are indeed limited in the degree to which they can evolve into new environmental conditions.

Climate change and vector-borne diseases.

In this review we examine formally the conditions under which vector-borne diseases are likely to change, and the directions of those changes, under various scenarios of climate change. We specify the criteria that must be met in order to conclude that climate change is having an effect on vector-borne diseases. We then take several examples from the literature and show how some of them meet these criteria, while others do not. For those that do not, there are alternative explanations that involve much more plausible drivers of the recorded changes in the diseases concerned.

Global transport networks and infectious disease spread.

Air, sea and land transport networks continue to expand in reach, speed of travel and volume of passengers and goods carried. Pathogens and their vectors can now move further, faster and in greater numbers than ever before. Three important consequences of global transport network expansion are infectious disease pandemics, vector invasion events and vector-borne pathogen importation. This review briefly examines some of the important historical examples of these disease and vector movements, such as the global influenza pandemics, the devastating Anopheles gambiae invasion of Brazil and the recent increases in imported Plasmodium falciparum malaria cases. We then outline potential approaches for future studies of disease movement, focussing on vector invasion and vector-borne disease importation. Such approaches allow us to explore the potential implications of international air travel, shipping routes and other methods of transport on global pathogen and vector traffic.

Population ecology of Heteronyx piceus (Coleoptera: Scarabaeidae) in a peanut/maize cropping system.

Large larval populations of the scarabaeid beetle Heteronyx piceus Blanchard that occur under peanuts, but not maize, in the South Burnett region of Australia are the result of a high rate and prolonged period of egg production by females feeding on peanut foliage. Heteronyx piceus is a relatively sedentary species and movement of females between adjacent fields is low. Populations of H. piceus varied markedly with landscape position. High larval populations are more likely (1 in 4 chance) to be encountered on the 'scrub' soils in the upper parts of the landscape than in the 'forest' soils in the lower half (1 in 20 chance), indicating that soil type/landscape position is a key risk factor in assessing the need for management intervention. The studies indicate that, because of the species' sedentary nature, the most meaningful population entity for management of H. piceus is the individual field, rather than the whole-farm or the region. The implications of this population ecology for management of the pest are discussed in relation to control strategies.

Modelling malaria risk in East Africa at high-spatial resolution.

OBJECTIVES: Malaria risk maps have re-emerged as an important tool for appropriately targeting the limited resources available for malaria control. In Sub-Saharan Africa empirically derived maps using standardized criteria are few and this paper considers the development of a model of malaria risk for East Africa. METHODS: Statistical techniques were applied to high spatial resolution remotely sensed, human settlement and land-use data to predict the intensity of malaria transmission as defined according to the childhood parasite ratio (PR) in East Africa. Discriminant analysis was used to train environmental and human settlement predictor variables to distinguish between four classes of PR risk shown to relate to disease outcomes in the region. RESULTS: Independent empirical estimates of the PR were identified from Kenya, Tanzania and Uganda (n = 330). Surrogate markers of climate recorded on-board earth orbiting satellites, population settlement, elevation and water bodies all contributed significantly to the predictive models of malaria transmission intensity in the sub-region. The accuracy of the model was increased by stratifying East Africa into two ecological zones. In addition, the inclusion of urbanization as a predictor of malaria prevalence, whilst reducing formal accuracy statistics, nevertheless improved the consistency of the predictive map with expert opinion malaria maps. The overall accuracy achieved with ecological zone and urban stratification was 62% with surrogates of precipitation and temperature being among the most discriminating predictors of the PR. CONCLUSIONS: It is possible to achieve a high degree of predictive accuracy for Plasmodium falciparum parasite prevalence in East Africa using high-spatial resolution environmental data. However, discrepancies were evident from mapped outputs from the models which were largely due to poor coverage of malaria training data and the comparable spatial resolution of predictor data. These deficiencies will only be addressed by more random, intensive small areas studies of empirical estimates of PR.

Modelling the distributions of Culicoides bluetongue virus vectors in Sicily in relation to satellite-derived climate variables.

Surveillance data from 268 sites in Sicily are used to develop climatic models for prediction of the distribution of the main European bluetongue virus (BTV) vector Culicoides imicola Kieffer (Diptera: Ceratopogonidae) and of potential novel vectors, Culicoides pulicaris Linnaeus, Culicoides obsoletus group Meigen and Culicoides newsteadi Austen. The models containing the 'best' climatic predictors of distribution for each species, were selected from combinations of 40 temporally Fourier-processed remotely sensed variables and altitude at a 1 km spatial resolution using discriminant analysis. Kappa values of around 0.6 for all species models indicated substantial levels of agreement between model predictions and observed data. Whilst the distributions of C. obsoletus group and C. newsteadi were predicted by temperature variables, those of C. pulicaris and C. imicola were determined mainly by normalized difference vegetation index (NDVI), a variable correlated with soil moisture and vegetation biomass and productivity. These models were used to predict species presence in unsampled pixels across Italy and for C. imicola across Europe and North Africa. The predicted continuous presence of C. pulicaris along the appenine mountains, from north to south Italy, suggests BTV transmission may be possible in a large proportion of this region and that seasonal transhumance (seasonal movement of livestock between upland and lowland pastures) even in C. imicola-free areas should not generally be considered safe. The predicted distribution of C. imicola distribution shows substantial agreement with observed surveillance data from Greece and Iberia (including the Balearics) and parts of mainland Italy (Lazio, Tuscany and areas of the Ionian coast) but is generally much more restricted than the observed distribution (in Sardinia, Corsica and Morocco). The low number of presence sites for C. imicola in Sicily meant that only a restricted range of potential C. imicola habitats were included in the training set and that predictions could only be made within this range. Future modelling exercises will use abundance data collected according to a standardized protocol across the Mediterranean and, for Sicily in particular, should include non-climatic environmental variables that may influence breeding site suitability such as soil type.

Predicting the risk of bluetongue through time: climate models of temporal patterns of outbreaks in Israel.

Determining the temporal relationship between climate and epidemics of Culicoides-borne viral disease may allow control and surveillance measures to be implemented earlier and more efficiently. In Israel, outbreaks of bluetongue (BT) have occurred almost annually since at least 1950, with severe episodes occurring periodically. In this paper, the authors model a twenty-year time-series of BT outbreaks in relation to climate. Satellite-derived correlates of low temperatures and high moisture levels increased the number of outbreaks per year. This is the first study to find a temporal relationship between the risk of Culicoides-borne disease and satellite-derived climate variables. Climatic conditions in the year preceding a BT episode, between October and December, coincident with the seasonal peak of vector abundance and outbreak numbers, appeared to be more importantthan spring or early summer conditions in the same year as the episode. Since Israel is an arid country, higher-than-average moisture levels during this period may increase the availability of breeding sites and refuges for adult Culicoides imicola vectors, while cooler-than-average temperatures will increase fecundity, offspring size and survival through adulthood in winter, which, in turn, increases the size of the initial vector population the following year. The proportion of variance in the annual BT outbreak time-series resulting from climate factors was relatively low, at around 20%. This was possibly due to temporal variation in other factors, such as viral incursions from surrounding countries and levels of herd immunity. Alternatively, since most BT virus (BTV) circulation in this region occurs silently, in resistant breeds of local sheep, the level of transmission is poorly correlated with outbreak notification so that strong relationships between BTV circulation and climate, if they exist, are obscured.

What factors determine when epidemics occur in the Mediterranean? Prediction of disease risk through time by climate-driven models of the temporal distribution of outbreaks in Israel.

Determination of the temporal relationships between climate and epidemics of Culicoides-borne viral disease may lead to control measures and surveillance being implemented earlier and more efficiently. Although Israel has reported few cases of bluetongue (BT) during the recent Mediterranean epidemic, outbreaks have occurred almost annually since the disease was first confirmed there (1950) with severe episodes occurring periodically. The south Mediterranean location and intensive farming of BT-susceptible European sheep breeds make the area ideal for investigation of the effect or role of climatic factors versus other potential host or virus factors in governing the timing of severe BT episodes. The authors present regression analyses of 20-year time-series of BT outbreaks versus four remotely sensed climatic variables. Low temperatures and high moisture levels (relative to average levels) in the preceding autumn coincident with the seasonal peak of vector abundance and outbreaks had a positive effect on the number of outbreaks the following year. The positive effects of high moisture levels are postulated to increase breeding site availability and refugia for adult C. imicola vectors (from desiccation) in autumn whilst low temperatures may increase fecundity, offspring size and survival through adulthood in winter by increasing initial vector population size the following year. The proportion of variance in the annual BT outbreak time series accounted for by climate factors was relatively low (approximately 20%), probably because most BT virus (BTV) circulation occurs silently, due to the circulation of non-virulent BTV strains, combined with the prevalence of relatively resistant local sheep breeds. Thus, the level of BTV transmission is poorly correlated with the rate of outbreak notification.

Modelling the distribution of outbreaks and Culicoides vectors in Sicily: towards predictive risk maps for Italy.

Vector (911 light-trap catches from 269 sites) and serological surveillance data were obtained during recent bluetongue (BT) outbreaks in Sicily. The distributions of Culicoides vectors are compared with that of bluetongue virus (BTV) to determine the relative role of different vectors in BTV transmission in Sicily. The 'best' climatic predictors of distribution for each vector species were selected from 40 remotely-sensed variables and altitude at a 1 km spatial resolution using discriminant analysis. These models were used to predict species presence in unsampled pixels across Italy. Although Culicoides imicola, the main European vector, was found in only 12% of sites, there was close correspondence between its spatial distribution and that of the 2000 and 2001 outbreaks. All three candidate vectors C. pulicaris, C. newsteadi and C. obsoletus group were widespread across 2002 outbreak sites but C. newsteadi was significantly less prevalent in outbreak versus non-outbreak sites in Messina and BTV has been isolated from wild-caught adults of both C. pulicaris and C. obsoletus in Italy. The yearly distribution and intensity of outbreaks is attributable to the distribution and abundance of the vectors operating in each year. Outbreaks were few and coastal in 2000 and 2001 due to the low abundance and prevalence of the vector, C. imicola. They were numerous and widespread in 2002, following hand-over of the virus to more prevalent and abundant novel vector species, C. pulicaris and C. obsoletus. Climatic determinants of distribution were species-specific, with those of C. obsoletus group and C. newsteadi predicted by temperature variables, and those of C. pulicaris and C. imicola determined mainly by normalised difference vegetation index (NDVI), a variable correlated with soil moisture, vegetation biomass and productivity. The predicted continuous presence of C. pulicaris along the Appenine mountains, from north to south Italy, suggests BTV transmission may be possible in a large proportion of this region and that seasonal transhumance between C. imicola-free areas should not generally be considered safe. Future distribution models for C. imicola in Sicily should include non-climatic environmental variables that may influence breeding site suitability such as soil type.

Prediction of bluetongue vector distribution in Europe and north Africa using satellite imagery.

Bluetongue is an infectious, non-contagious arboviral disease thought to infect all known ruminant species. Since 1998, an unprecedented epizootic of the disease has occurred in the Mediterranean region, resulting in the deaths of over 800,000 sheep to date. Bluetongue virus (BTV) is transmitted by biting midges of which one species, Culicoides imicola, is the major vector in the old world. C. imicola was trapped for 2 years at 87 sites across Portugal and models were developed for predicting the presence and abundance of the midge at these sites. Discriminant analysis was used to identify the best models from 40 temporally Fourier-processed 1 km spatial resolution remotely-sensed variables. The best models correctly predicted presence and absence at 83 of the 87 sites, and abundance at 76 sites. The models were then used to predict C. imicola presence and abundance elsewhere across Europe and north Africa. C. imicola was predicted to be present and in high abundance at the majority of areas affected in the recent bluetongue epizootic, including the Balearics, Sardinia, Corsica, Sicily, areas of mainland Italy, large areas of Greece, western Turkey and northern Algeria and Tunisia.

Updating Historical Maps of Malaria Transmission Intensity in East Africa Using Remote Sensing.

Remotely sensed imagery has been used to update and improve the spatial resolution of malaria transmission intensity maps in Tanzania, Uganda, and Kenya. Discriminant analysis achieved statistically robust agreements between historical maps of the intensity of malaria transmission and predictions based on multitemporal meteorological satellite sensor data processed using temporal Fourier analysis. The study identified land surface temperature as the best predictor of transmission intensity. Rainfall and moisture availability as inferred by cold cloud duration (ccd) and the normalized difference vegetation index (ndvi), respectively, were identified as secondary predictors of transmission intensity. Information on altitude derived from a digital elevation model significantly improved the predictions. "Malaria-free" areas were predicted with an accuracy of 96 percent while areas where transmission occurs only near water, moderate malaria areas, and intense malaria transmission areas were predicted with accuracies of 90 percent, 72 percent, and 87 percent, respectively. The importance of such maps for rationalizing malaria control is discussed, as is the potential contribution of the next generation of satellite sensors to these mapping efforts.