Operationalising the "One Health" approach in India: facilitators of and barriers to effective cross-sector convergence for zoonoses prevention and control.

BACKGROUND: There is a strong policy impetus for the One Health cross-sectoral approach to address the complex challenge of zoonotic diseases, particularly in low/lower middle income countries (LMICs). Yet the implementation of this approach in LMIC contexts such as India has proven challenging, due partly to the relatively limited practical guidance and understanding on how to foster and sustain cross-sector collaborations. This study addresses this gap by exploring the facilitators of and barriers to successful convergence between the human, animal and environmental health sectors in India. METHODS: A mixed methods study was conducted using a detailed content review of national policy documents and in-depth semi-structured interview data on zoonotic disease management in India. In total, 29 policy documents were reviewed and 15 key informant interviews were undertaken with national and state level policymakers, disease managers and experts operating within the human-animal-environment interface of zoonotic disease control. RESULTS: Our findings suggest that there is limited policy visibility of zoonotic diseases, although global zoonoses, especially those identified to be of pandemic potential by international organisations (e.g. CDC, WHO and OIE) rather than local, high burden endemic diseases, have high recognition in the existing policy agenda setting. Despite the widespread acknowledgement of the importance of cross-sectoral collaboration, a myriad of factors operated to either constrain or facilitate the success of cross-sectoral convergence at different stages (i.e. information-sharing, undertaking common activities and merging resources and infrastructure) of cross-sectoral action. Importantly, participants identified the lack of supportive policies, conflicting departmental priorities and limited institutional capacities as major barriers that hamper effective cross-sectoral collaboration on zoonotic disease control. Building on existing informal inter-personal relationships and collaboration platforms were suggested by participants as the way forward. CONCLUSION: Our findings point to the importance of strengthening existing national policy frameworks as a first step for leveraging cross-sectoral capacity for improved disease surveillance and interventions. This requires the contextual adaptation of the One Health approach in a manner that is sensitive to the underlying socio-political, institutional and cultural context that determines and shapes outcomes of cross-sector collaborative arrangements.

Modelling the effect of temperature on the seasonal population dynamics of temperate mosquitoes.

Mosquito-borne diseases cause substantial mortality and morbidity worldwide. These impacts are widely predicted to increase as temperatures warm and extreme precipitation events become more frequent, since mosquito biology and disease ecology are strongly linked to environmental conditions. However, direct evidence linking environmental change to changes in mosquito-borne disease is rare, and the ecological mechanisms that may underpin such changes are poorly understood. Environmental drivers, such as temperature, can have non-linear, opposing impacts on the demographic rates of different mosquito life cycle stages. As such, model frameworks that can deal with fluctuations in temperature explicitly are required to predict seasonal mosquito abundance, on which the intensity and persistence of disease transmission under different environmental scenarios depends. We present a novel, temperature-dependent, delay-differential equation model, which incorporates diapause and the differential effects of temperature on the duration and mortality of each life stage and demonstrates the sensitivity of seasonal abundance patterns to inter- and intra-annual changes in temperature. Likely changes in seasonal abundance and exposure to mosquitoes under projected changes in UK temperatures are presented, showing an increase in peak vector abundance with warming that potentially increases the risk of disease outbreaks.

Bionomics of temperate and tropical Culicoides midges: knowledge gaps and consequences for transmission of Culicoides-borne viruses.

Culicoides midges are abundant hematophagous flies that vector arboviruses of veterinary and medical importance. Dramatic changes in the epidemiology of Culicoides-borne arboviruses have occurred since 1998, including the emergence of exotic viruses in northern temperate regions, increases in global disease incidence, and enhanced virus diversity in tropical zones. Drivers may include changes in climate, land use, trade, and animal husbandry. New Culicoides species and new wild reservoir hosts have been implicated in transmission, highlighting the dynamic nature of pathogen-vector-host interactions. Focusing on potential vector species worldwide and key elements of vectorial capacity, we review the sensitivity of Culicoides life cycles to abiotic and biotic factors. We consider implications for designing control measures and understanding impacts of environmental change in different ecological contexts. Critical geographical, biological, and taxonomic knowledge gaps are prioritized. Recent developments in genomics and mathematical modeling may enhance ecological understanding of these complex arbovirus systems.

Land system governance shapes tick-related public and animal health risks.

Land cover and land use have established effects on hazard and exposure to vector-borne diseases. While our understanding of the proximate and distant causes and consequences of land use decisions has evolved, the focus on the proximate effects of landscape on disease ecology remains dominant. We argue that land use governance, viewed through a land system lens, affects tick-borne disease risk. Governance affects land use trajectories and potentially shapes landscapes favourable to ticks or increases contact with ticks by structuring human-land interactions. We illustrate the role of land use legacies, trade-offs in land-use decisions, and social inequities in access to land resources, information and decision-making, with three cases: Kyasanur Forest disease in India, Lyme disease in the Outer Hebrides (Scotland), and tick acaricide resistance in cattle in Ecuador. Land use governance is key to managing the risk of tick-borne diseases, by affecting the hazard and exposure. We propose that land use governance should consider unintended consequences on infectious disease risk.

Larval development and emergence sites of farm-associated Culicoides in the United Kingdom.

Culicoides biting midges (Diptera: Ceratopogonidae) are the biological vectors of internationally important arboviruses of livestock including bluetongue virus (BTV). Information on the habitats used by Culicoides for larval development is valuable for establishing targeted vector control strategies and for improving local scale models of vector abundance. This study combines emergence trap collections of adult Culicoides identified using molecular markers and physiochemical measurements of habitats to investigate larval development sites of Palaearctic Culicoides in South East England. The known range of larval habitats for several Culicoides species is extended and the potential BTV vector species C. obsoletus and C. scoticus are confirmed to co-occur in many larval habitats. The presence of emerging C. obsoletus was favoured by increasing substrate moisture level [odds ratio (OR) 6.94 (2.30; 20.90)] and substrate pH [OR 4.80 (1.66; 13.90)] [bias-corrected Dxy : 0.68; area under the curve (AUC): 0.86] rather than any particular larval habitat type, as expected for a species with relatively wide larval habitat preference. Of the newly emerged sub-genus Avaritia individuals collected, 23% were observed to have a degree of abdominal pigmentation commonly inferred to indicate parity. If consistent across species and locations, this observation represents a potential source of error for age structure analyses of Culicoides populations.

Identifying environmental drivers of insect phenology across space and time: Culicoides in Scotland as a case study.

Interpreting spatial patterns in the abundance of species over time is a fundamental cornerstone of ecological research. For many species, this type of analysis is hampered by datasets that contain a large proportion of zeros, and data that are overdispersed and spatially autocorrelated. This is particularly true for insects, for which abundance data can fluctuate from zero to many thousands in the space of weeks. Increasingly, an understanding of the ways in which environmental variation drives spatial and temporal patterns in the distribution, abundance and phenology of insects is required for management of pests and vector-borne diseases. In this study, we combine the use of smoothing techniques and generalised linear mixed models to relate environmental drivers to key phenological patterns of two species of biting midges, Culicoides pulicaris and C. impunctatus, of which C. pulicaris has been implicated in transmission of bluetongue in Europe. In so doing, we demonstrate analytical tools for linking the phenology of species with key environmental drivers, despite using a relatively small dataset containing overdispersed and zero-inflated data. We demonstrate the importance of landcover and climatic variables in determining the seasonal abundance of these two vector species, and highlight the need for more empirical data on the effects of temperature and precipitation on the life history traits of palearctic Culicoides spp. in Europe.

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.

Impacts of climate, host and landscape factors on Culicoides species in Scotland.

Culicoides biting midges (Diptera: Ceratopogonidae) vector a wide variety of internationally important arboviral pathogens of livestock and represent a widespread biting nuisance. This study investigated the influence of landscape, host and remotely-sensed climate factors on local abundance of livestock-associated species in Scotland, within a hierarchical generalized linear model framework. The Culicoides obsoletus group and the Culicoides pulicaris group accounted for 56% and 41%, respectively, of adult females trapped. Culicoides impunctatus Goetghebuer and C. pulicaris s.s. Linnaeus were the most abundant and widespread species in the C. pulicaris group (accounting for 29% and 10%, respectively, of females trapped). Abundance models performed well for C. impunctatus, Culicoides deltus Edwards and Culicoides punctatus Meigen (adjusted R(2) : 0.59-0.70), but not for C. pulicaris s.s. (adjusted R(2) : 0.36) and the C. obsoletus group (adjusted R(2) : 0.08). Local-scale abundance patterns were best explained by models combining host, landscape and climate factors. The abundance of C. impunctatus was negatively associated with cattle density, but positively associated with pasture cover, consistent with this species' preference in the larval stage for lightly grazed, wet rush pasture. Predicted abundances of this species varied widely among farms even over short distances (less than a few km). Modelling approaches that may facilitate the more accurate prediction of local abundance patterns for a wider range of Culicoides species are discussed.

Livestock host composition rather than land use or climate explains spatial patterns in bluetongue disease in South India.

Culicoides-borne arboviruses of livestock impair animal health, livestock production and livelihoods worldwide. As these arboviruses are multi-host, multi-vector systems, predictions to improve targeting of disease control measures require frameworks that quantify the relative impacts of multiple abiotic and biotic factors on disease patterns. We develop such a framework to predict long term (1992-2009) average patterns in bluetongue (BT), caused by bluetongue virus (BTV), in sheep in southern India, where annual BT outbreaks constrain the livelihoods and production of small-holder farmers. In Bayesian spatial general linear mixed models, host factors outperformed landscape and climate factors as predictors of disease patterns, with more BT outbreaks occurring on average in districts with higher densities of susceptible sheep breeds and buffalo. Since buffalo are resistant to clinical signs of BT, this finding suggests they are a source of infection for sympatric susceptible sheep populations. Sero-monitoring is required to understand the role of buffalo in maintaining BTV transmission and whether they must be included in vaccination programs to protect sheep adequately. Landscape factors, namely the coverage of post-flooding, irrigated and rain-fed croplands, had weak positive effects on outbreaks. The intimate links between livestock host, vector composition and agricultural practices in India require further investigation at the landscape scale.

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.

Understanding Spatio-Temporal Variability in the Reproduction Ratio of the Bluetongue (BTV-1) Epidemic in Southern Spain (Andalusia) in 2007 Using Epidemic Trees.

Andalusia (Southern Spain) is considered one of the main routes of introduction of bluetongue virus (BTV) into Europe, evidenced by a devastating epidemic caused by BTV-1 in 2007. Understanding the pattern and the drivers of BTV-1 spread in Andalusia is critical for effective detection and control of future epidemics. A long-standing metric for quantifying the behaviour of infectious diseases is the case-reproduction ratio (Rt), defined as the average number of secondary cases arising from a single infected case at time t (for t>0). Here we apply a method using epidemic trees to estimate the between-herd case reproduction ratio directly from epidemic data allowing the spatial and temporal variability in transmission to be described. We then relate this variability to predictors describing the hosts, vectors and the environment to better understand why the epidemic spread more quickly in some regions or periods. The Rt value for the BTV-1 epidemic in Andalusia peaked in July at 4.6, at the start of the epidemic, then decreased to 2.2 by August, dropped below 1 by September (0.8), and by October it had decreased to 0.02. BTV spread was the consequence of both local transmission within established disease foci and BTV expansion to distant new areas (i.e. new foci), which resulted in a high variability in BTV transmission, not only among different areas, but particularly through time, which suggests that general control measures applied at broad spatial scales are unlikely to be effective. This high variability through time was probably due to the impact of temperature on BTV transmission, as evidenced by a reduction in the value of Rt by 0.0041 for every unit increase (day) in the extrinsic incubation period (EIP), which is itself directly dependent on temperature. Moreover, within the range of values at which BTV-1 transmission occurred in Andalusia (20.6°C to 29.5°C) there was a positive correlation between temperature and Rt values, although the relationship was not linear, probably as a result of the complex relationship between temperature and the different parameters affecting BTV transmission. Rt values for BTV-1 in Andalusia fell below the threshold of 1 when temperatures dropped below 21°C, a much higher threshold than that reported in other BTV outbreaks, such as the BTV-8 epidemic in Northern Europe. This divergence may be explained by differences in the adaptation to temperature of the main vectors of the BTV-1 epidemic in Andalusia (Culicoides imicola) compared those of the BTV-8 epidemic in Northern Europe (Culicoides obsoletus). Importantly, we found that BTV transmission (Rt value) increased significantly in areas with higher densities of sheep. Our analysis also established that control of BTV-1 in Andalusia was complicated by the simultaneous establishment of several distant foci at the start of the epidemic, which may have been caused by several independent introductions of infected vectors from the North of Africa. We discuss the implications of these findings for BTV surveillance and control in this region of Europe.

Quantifying the Risk of Introduction of West Nile Virus into Great Britain by Migrating Passerine Birds.

West Nile virus (WNV) is a mosquito borne arbovirus that circulates within avian reservoirs. WNV can spill over into humans and Equidae that are dead-end hosts for WNV but suffer fever, acute morbidity and sometimes death. Outbreaks of WNV are common across Africa and Eastern Europe, and there have also been sporadic outbreaks in Spain and the Camargue Regional Park in France, but never in Great Britain (GB). These areas all fall along a major bird migration route. In this study, we analyse a scenario in which WNV is circulating in the Camargue or in other wetland areas in France and we estimate the risk of northward migrating passerine birds stopping in a WNV hotspot, becoming infected and carrying active infection to GB. If the disease were circulating in the Camargue during a single migratory season, the probability that one or more migrating birds becomes infected and lands in GB whilst still infected is 0.881 with 0.384 birds arriving in areas of suitable vector habitat. However, if WNV became established in the Grand Brière National Park or La Brenne Regional Park wetland areas further to the north, the model predicts that at least one infected bird will continue to GB. Thus, GB is at risk of WNV introduction from the Camargue, but the risk is considerably greater if WNV were to circulate further north than its previous focus in France, but this is highly sensitive to the force of infection in the infected area. However, the risk of establishment and infection of humans in GB is dependent upon a number of additional factors, in particular the vector and epidemiological situation in GB.

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.

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.

Does covering of farm-associated Culicoides larval habitat reduce adult populations in the United Kingdom?

Culicoides biting midges (Diptera: Ceratopogonidae) are the biological vectors of a range of internationally important arboviruses of livestock, including bluetongue virus (BTV) and the recently emerging Schmallenberg virus (SBV). Culicoides species in the subgenus Avaritia (in the UK: Culicoides obsoletus Meigen, Culicoides scoticus Downes & Kettle, Culicoides dewulfi Goetghebuer and Culicoides chiopterus Meigen) have been implicated in BTV transmission in northern Europe and to a varying degree utilise cattle dung as a larval development substrate. The collection of cattle dung into heaps on farms provides a localised source of Culicoides emergence in close proximity to livestock. This study assesses the impact of covering dung heaps prior to the onset of adult Culicoides activity with the aim of reducing recruitment to the local adult populations at four livestock farms in England. Light suction trap catches of adult Culicoides from these farms were compared with those from four untreated control farms from a wide geographic range across the UK. It was demonstrated that implementing control of emergence from dung heaps did not have a significant impact upon the local adult subgenus Avaritia abundance at the treated farm holdings and that the onset of Culicoides activity was similarly unaffected. Use of this method in isolation is unlikely to have an effect in reducing the risk of BTV and SBV transmission. The implications of these results for control of farm-associated Culicoides in Europe are discussed.

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.

Quantifying the wind dispersal of Culicoides species in Greece and Bulgaria.

This paper tests the hypothesis that Culicoides (Diptera: Ceratopogonidae) species can be propagated by wind over long distances. Movement patterns of midges were inferred indirectly from patterns of the spread of bluetongue outbreaks between farms (using outbreak data from 1999-2001 for Greece, Bulgaria and Turkey) and then matched to concurrent wind patterns. The general methodology was to determine wind trajectories to and from each outbreak site based on the horizontal and vertical wind components of the European ReAnalysis-40 (ERA-40) dataset from the European centre for medium-range weather forecast (ECMWF). Forward trajectories (downwind or where the windvectors pointed to) and backward trajectories (upwind or where the wind-vectors originated from) were calculated for each outbreak for the period from one week before to one week after it had been recorded. These wind trajectories were then compared with the general outbreak patterns taking into consideration the different serotypes involved. It was found that the wind trajectories could be matched to the temporal distribution of the outbreak cases. Furthermore, the spread of the infected vector via the calculated wind trajectories was corroborated by molecular evidence. The conclusion is that the methodology presented is appropriate for quantifying the risk of spread of infected Culicoides midges by wind and that this approach could form an important component of a regional early-warning system for bluetongue.

Spatial and temporal distribution of bluetongue and its Culicoides vectors in Bulgaria.

Surveillance of Culicoides (Diptera: Ceratopogonidae) biting midges was carried out between 2001 and 2003, at 119 sites within a 50 x 50-km grid distributed across Bulgaria, using light trap collections around the time of peak adult midge abundance. Sentinel and ad hoc serum surveillance of hosts susceptible to bluetongue infection was carried out at around 300 sites between 1999 and 2003. Following the initial incursion of bluetongue virus 9 (BTV-9) into Bourgas province in 1999, affecting 85 villages along the southern border, a further 76 villages were affected along the western border in 2001, with outbreaks extending as far north as 43.6 degrees N. The BTV-9 strain in circulation was found to have a low pathogenicity for Bulgarian sheep populations, with less than 2% of susceptible individuals becoming sick and seroconversions detected up to 30 km from recorded outbreaks in the south. The major Old World vector Culicoides imicola Kieffer was not detected among over 70,000 Culicoides identified in summer collections, suggesting that BTV-9 transmission in Bulgaria was primarily carried out by indigenous European vectors. The most likely candidates, the Palaearctic species complexes - the Culicoides obsoletus Meigen and C. pulicaris L. complexes - were widespread and abundant across the whole country. The C. obsoletus complex represented 75% of all individuals trapped in summer and occurred in high catch sizes (up to 15,000 individuals per night) but was not found across all outbreak sites, indicating that both Palearctic complexes probably played a role in transmission. Within the C. pulicaris complex, only C. pulicaris s.s., C. punctatus Meigen and C. newsteadi Austen were sufficiently abundant and prevalent to have been widely involved in transmission, whilst within the C. obsoletus complex most trapped males were C. obsoletus s.s. Adult vectors were found to be largely absent from sites in west Bulgaria for a period of at least 3 months over winter, which, taken along with the spatiotemporal pattern of outbreaks in the region between years, indicates the virus may be overwintering here by an alternative mechanism - either by covert persistence in the vertebrate host or possibly by persistence in larval stages of the vector.

Modelling the distribution of bluetongue vectors.

Recent epizootics of Culicoides-borne disease in the Mediterranean Basin have stimulated the development of climate-driven models for vectors. Predictor variables come from two main sources, weather data and satellites. Generally, models for Culicoides imicola combine temperature and moisture variables. The best weather models explain 75-85% of the variance in observed data for C. imicola, but satellite models perform better (85-95% of variance). Predictions of models for other regions appear mixed, with successes and failures. The failures indicate the need to: explore and incorporate other factors that may affect Culicoides populations, such as soil characteristics, host type and wind speed. Develop more complex models, recognising that different climate variables affect different stages of the life-cycle e.g. biological models. The very rapid spread in the distribution of C. imicola in recent years suggests that global warming may be a less important driver of change than other, currently unknown, factors.