Monitoring and Intervention Strategies for Bluetongue Virus Epidemics in Rural India

Lead Research Organisation: NERC Centre for Ecology and Hydrology
Department Name: Watt

Abstract

Bluetongue virus (BTV) is an arboviral pathogen of ruminants spread by Culicoides biting midges, which causes the disease bluetongue (BT) in sheep (particularly certain fine wool and mutton breeds). During the 1980's clinical BT began to appear in flocks of native Indian breeds of sheep, particularly in the southern states, possibly as a result of exotic strains of the virus introduced via sheep-breeding programmes. This change in epidemiology led to outbreaks among family-based subsistence farming communities in these areas, and BTV has since been become a significant constraint in both the rearing and productivity of indigenous flocks. In addition, in rain-fed agricultural areas, massive periodic outbreaks of disease occur that are thought to be related to the influence of timing and intensity of monsoon conditions on populations of vectors responsible for spreading BTV. Due to the circulation of 21 serotypes of BTV in southern India and the prohibitive costs of vaccination to the vast majority of the population, vector control remains the only feasible way of combating BTV transmission in the field. Despite this, virtually no quantitative data concerning the efficiency of available techniques in this role is available to inform control strategies. We will adopt a multidisciplinary approach involving mathematical modelling, entomology and chemical ecology to examine the epidemiology of BTV in the southern Indian states and to produce prediction, monitoring and mitigation techniques that can reduce the impact of BT in this region. Initially we will characterise southern India using mapping techniques that delineate land areas according to climate and land use patterns. We will then establish field sites across the region that are representative of both these factors and also the types of husbandry employed (with an emphasis on small holdings and landless husbandry workers). Having characterised these sites, we will then use light trapping to define adult seasonality and distribution and ground truth this survey with direct collection of Culicoides from livestock. These studies will be combined with detection of BTV within collected individual midges to define regional variation in which species are involved in transmission in southern India for the first time. The larval development sites of major vector species identified will then also be characterised via field investigations. Using data generated on adult seasonality, larval habitat preference and historic surveys of BT cases across southern India, we will then model the relationship between monsoon conditions and adult Culicoides/BT activity to assess the potential to produce an early warning system for major BTV epidemics based on meteorological variables. The provision of fundamental epidemiological knowledge will also enable an assessment of husbandry-based control techniques for Culicoides that could be employed to reduce BTV transmission by subsistence farmers in a cost-neutral fashion. We will examine traditional and novel means of control, both in the laboratory and in the field. The former will include the use of larval site modification, or targeted treatment with traditional, low environmental impact, insecticidal products available to villagers and additionally the use of stabling. In addition, information regarding host location by identified vector Culicoides will allow novel intervention strategies based upon the application of masking semiochemicals that could also reduce the use of synthetic insecticides by these communities in the medium term. The effect of combinations of these techniques will be examined via monitoring viral infection in livestock, as a gold standard for evidence of impact in the field. These data will then be assessed for integration into the everyday lives of user groups as part of wider dissemination frameworks for improvement of ruminant productivity and control of vectors of human and veterinary pathogens.

Technical Summary

This project takes a multidisciplinary approach to understanding epidemiology of the ruminant disease, bluetongue (BT), in India, with a view to developing tools for accurate risk assessment and appropriate, low-cost vector control. In India bluetongue virus (BTV) imposes the major constraint on sheep rearing - with subsistence farming communities in the south being most severely affected due to periodic, monsoon-driven hyperendemic outbreaks. Vector control is currently the only option for disease management, since co-circulation of many BTV strains and expense of vaccines render protective immunisation unachievable. Our team combines specialists in veterinary medicine, entomology, chemical ecology, ecological modelling and remote sensing with long term surveillance datasets and field-based experiments to deliver for India, the first assessment of key midge vectors involved in transmission, an in-depth understanding of the environmental conditions that drive midge population increases and that, in turn, drive the timing and locations of BT epidemics and hyper-epidemics, as well as a thorough evaluation of current and novel technology for vector surveillance and control. These will be integrated into a framework for risk assessment of BTV epidemics and design of optimal strategies for low cost vector control.

Planned Impact

The main beneficiaries of the knowledge generated by this project fall into three main groups (listed in order of importance): 1. Subsistence sheep farming communities living within rain-fed agricultural systems in southern India that cannot afford the use of vaccination for bluetongue virus. Through a detailed dissemination plan, our project will provide this group with: (a) advice on optimal husbandry methods for minimising the likelihood of BTV transmission (b) knowledge on when the 'high-risk' transmission period is likely to occur in their region (c) information on how to delineate and remove midge breeding sites (targeted at key vector species) in and around farms (d) advice on the effectiveness and practical implementation of existing and new, low cost, vector control measures to reduce midge populations The widespread uptake of low cost, environmentally friendly vector control options would bring benefits for biodiversity and human health in India in the short to medium term. 2. Larger operators for which immunisation of stock with newly developed vaccines might be practical in the medium term. Early warning systems of major BTV epidemics have the potential to be used to increase uptake of vaccines and hence ameliorate the worst effects of outbreaks. 3. Policy makers responsible for managing bluetongue across India and the academic community including vector control specialists, epidemiologists and veterinarians. This group will benefit from: (a) A ranking of the midge species in southern India by the importance they play in bluetongue virus transmission (b) A thorough understanding of the seasonal conditions favouring high abundance of key midge vectors and high levels of bluetongue virus transmission in India (c) An evaluation of the importance of monsoon conditions in driving hyperepidemic outbreaks of BTV (d) An evaluation of whether key vectors and common strains of bluetongue virus are favoured by different combinations of seasonal conditions (e) Regional scale predictive maps showing the distribution of suitable habitat for each key vector species (f) Regional scale predcitive maps showing the probable annual timing of transmission in different areas of southern India (g) Interactive tools for forecasting monsoon driven epidemics on the basis of annual meteorological conditions (h) Development of novel field techniques for midge control and surveillance (i) A paper-based assessment of new and existing field control techniques for midges in relation to (i) control options for other vectors and (ii) how these can be integrated into current farming practices of both large and small holders. Communication with small and large holders will be established through the Directorate of Information and Publications on Agriculture, which is part of ICAR, has huge experience in disseminating information to husbandry workers and will provide outlets for publicising the project in the media. In addition to exchanging information directly with farmers in the field study in southern India, project results will be published in trade magazines and leaflets and through the media, in addition to peer-review articles. During field visits to India, seminars will be carried out by the project team within institutions involved in the All India Network on Bluetongue and beyond (e.g. National Institute of Malaria Research, Delhi and the Vector Control Research Centre, Pondicherry). The wider academic community will be reached via publications (in open-access journals) and through presentations at international conferences. This will generate added value of providing useful training for the PhD student and PDRAs in dissemination activities. Expertise in remote sensing, GIS and predictive modelling of vector-borne diseases will be exchanged, primarily through the training of the project PhD student.
 
Description We have identified three key species of biting midge vectors that are most abundant and widespread across south India and therefore most likely to be involved in disease transmission. Furthermore, we have demonstrated that the adult vector season, during which animals are at risk from infection of bluetongue, varies significantly from place to place across south India and between key vector species. We are currently quantifying the monsoon, climate and host conditions under which adult vector seasons are prolonged or shortened or abundance levels increased, with the aim of guiding farmers and veterinary officers as to the probable length of the transmission season in different years and states.
Detailed questionnaire surveys of small-holder farmers across south India confirmed that bluetongue constitutes a top disease priority and helped us to identify suites of husbandry and vector control measures in common use that might impact development sites of biting midges and in turn increase (or decrease) exposure of susceptible sheep to bluetongue virus. This will contribute to tailored advice on vector control disseminated to farmers through leaflets and broadcasts of extension scientists from ICAR.
Key risk factors for bluetongue disease have been identified, by matching patterns in transmission with patterns in monsoon, host and climate conditions -over years and months and across districts and villages. Though monsoon rainfall increased the size of epidemics between years (state of Andhra Pradesh), disease severity varied substantially between districts within zones under similar monsoon conditions due to land use and host factors. More outbreaks occurred on average in districts with higher areas of post-flooding or irrigated croplands and rainfed croplands, probably because these land covers are more likely to contain suitable breeding habitat for biting midge vectors. Numbers of outbreaks also increased with some host types including local sheep breeds that may be more susceptible to BTV, and with buffalo densities, suggesting that the latter species may be an important reservoir species. These impacts varied between states, with the importance of buffalos and rice paddy land use being particularly significant for example in driving outbreaks in Andhra Pradesh. The risk maps and annual and monthly forecasts from these analyses at state, district and village level are being integrated into an early warning system for bluetongue disease that will be made publicly available in early 2015 and is tailored to needs of disease managers through consultation (using a workshop and questionnaire).
Exploitation Route Information on three key commonest vector species that are most likely involved in transmission in south India represents critical baseline data for ecological studies of habitat requirements of these species and subsequent development of tailored vector control methods by local entomologists. This together with insights from farmer questionnaires will contribute to tailored advice on vector control disseminated to farmers through leaflets and broadcasts of extension scientists from ICAR.
The risk maps and annual and monthly forecasts and understanding of risk factors from project analyses are being integrated into an early warning system for bluetongue disease that will be made publicly available in early 2015 and is tailored to needs of disease managers through consultation (using a workshop and questionnaire) - see narrative impact section.
The modelling approaches that we have used to link variability in monsoon conditions, hosts and landscape to bluetongue disease incidence and produce quantitative risk maps and forecasts is applicable to many of the top ranking animal health diseases in India, particularly those that are indirectly transmitted (liver fluke, Trypanosomiasis) or highly influenced by moisture levels (e.g Haemorrhagic Septicaemia, Black fever, para-Tuberculosis). Under the further funding, NERC National Capability project SUNRISE, we are working with the National Institute for Veterinary Epidemiology and Disease Informatics to apply these methods to a wider range of livestock and zoonotic diseases and to also investigate social factors affecting uptake and dissemination of forecasts.
Sectors Agriculture, Food and Drink,Communities and Social Services/Policy,Environment

URL http://www.IBVNet.com
 
Description In May 2014, we held a workshop to consult with disease managers on the value of the risk maps and forecasts and insights of disease risk factors arising from the IBVNet project (see Engagement). From this meeting, we ascertained that our forecasts of the timing of outbreaks could be used for ordering vaccines and preparing the vaccine schedule or "action plan" and to inform people about the likely severity of the outbreaks via a range of media It was thought that maps and forecasts might also help ministers to make policy decisions about disease control and obtain and allocate funds for vaccination and human resources. For example, animal marketing places are currently closed at soon as the first outbreaks are notified since mixing of large numbers of animals increases the risk of onward transmission. It was suggested that armed with forecasts of the kind generated by the IBVNet project, decisions to close animal markets and restrict animal movements could be made in advance of the transmission season. We ascertained the time scale and geographical resolution (district, state, village level) at which forecasts and risk maps would be of maximum value to them and the means by which they would prefer them to be communicated. These insights will be extremely valuable for tailoring IBVNet forecasts and risk maps to stakeholder needs when these are delivered in early 2015.
First Year Of Impact 2014
Sector Agriculture, Food and Drink
Impact Types Policy & public services

 
Description NERC Overseas Development Assistance National Capability Grant
Amount £7,000,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 07/2017 
End 03/2020
 
Title Agro-ecozonation for southern India to inform sampling strategy 
Description A key objective of WP1 is to produce a stratified agro-ecozonation for southern India to inform sampling strategy in work packages 2 to 5. Within the project as a whole we are looking at the role of climate, host and landscape factors on midge vector populations and BT epidemiology. However, a key focus of WP2 is to examine how whether geographical variation in the seasonality of different midge vectors can be explained by monsoon conditions. For this reason, it was felt to be most useful to produce a climate zonation, clustering areas by variation in monsoon conditions (particularly rainfall), that could then be overlaid with other key factors by which sample sites (forecast n=45) might be stratified. The overall aims of the ecozonation analysis then were to: • Divide southern India into zones reflecting differing monsoon conditions using different levels and methods of clustering • To assess whether the zonation produced is epidemiologically relevant. E.g. Does it delineate BT-affected and unaffected areas within states? Does it delineate areas with different seasonal profiles of BT cases? • Overlay climate zonation with other factors of epidemiological relevance (host distributions, land-cover and farm husbandry types) to inform vector sampling schemes. Consists of a zipped GIS file of ecozones (ecozonation.zip) and detailed documentation on the methodology (Ecozonation_for_south_India_for_the_CIDLID_project.pdf). Currently accessible only to project collaborators but available to anyone on request. https://wiki.ceh.ac.uk/display/blueindia/Trap+Distribution 
Type Of Material Database/Collection of data 
Year Produced 2013 
Provided To Others? No  
Impact No actual impacts realised to date 
URL https://wiki.ceh.ac.uk/display/blueindia/Trap+Distribution
 
Description CEH/ODA Foundation case for development (NERC National Capability) Promoting resilience to impacts of livestock and human pathogens 
Organisation Indian Council of Agricultural Research
Country India 
Sector Charity/Non Profit 
PI Contribution Under CEH's ODA Foundation Award from NERC, I received funding to lead a workpackage entitled "Promoting resilience to impacts of livestock and human pathogens". The funding supports establishment of a interdisciplinary partnership with ICAR-NIVEDI and linked Animal and Public Health research organisations in India to scope out extant forecasting systems for livestock and zoonotic diseases, to identify critical knowledge gaps and the potential for advancing forecasts by integrating novel statistics and wide ranging social, environmental and ecological drivers into forecasting models. We are also exploring whether forecasting methods can be generalised across diseases with similar traits. By engaging with key actors and beneficiaries at village, district, state and national scales during the Foundation phase, we are identifying the diseases of highest impact for which forecasts are most required. A key intended outcome of the partnership and research grants that build upon the Foundation Award will be reduction of disease burdens among small holder farmers in Lower Middle Income Countries by improved targeting of disease mitigation measures like vaccination, vector control and surveillance based on project forecasts This work builds on the methods and insight developed for bluetongue virus forecasting during BB/H009167/1.
Collaborator Contribution ICAR-NIVEDI provides epidemiological data and expertise, understanding of disease drivers and priorities and key linkage to policy makers and stakeholders impacted by livestock and zoonotic diseases and the work builds on their existing disease forecasting systems and frameworks such as NADRES.
Impact This collaboration is multi-disciplinary including ecological and epidemiological modelling, vector and pathogen ecology, Asian monsoon climatology, earth observation, and participatory research.
Start Year 2017
 
Description Stakeholder workshop: meeting of disease managers who may use project risk maps and outputs to improve bluetongue disease mitigation 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact A meeting of 25 stakeholders and disease managers was held, with participants drawn from across three states in south India that are worst affected by bluetongue disease. Officials with state-level, district-level and village-level responsibilities for bluetongue disease management were present. We presented the risk maps from the village to the district level that the project has generated as well as insights into key risk factors for bluetongue disease in each state. Through a questionnaire distributed to all participants followed by an open discussion we sought feedback on the value of the forecasts and risk maps for planning and mitigation measures at each geographical scale, preferred timing, formats and delivery mechanisms for forecasts/maps, and potential key risk factors that may be missing from our analyses. We also sought opinion on which critical pieces of scientific information would be most useful to disease maangers to improve mitigation.

From the stakeholder meeting, we ascertained that our forecasts of the timing of outbreaks could be used for ordering vaccines and preparing the vaccine schedule or "action plan" and to inform people about the likely severity of the outbreaks via a range of media (radio alerts, local TV, pamphlets and daily news papers). It was thought that maps and forecasts might also help ministers to make policy decisions about disease control and obtain and allocate funds for vaccination and human resources. For example, animal marketing places are currently closed at soon as the first outbreaks are notified since mixing of large numbers of animals increases the risk of onward transmission. It was suggested that armed with forecasts of the kind generated by the IBVNet project, decisions to close animal markets and restrict animal movements could be made in advance of the transmission season.
Stakeholders were also asked about the key risk factors for bluetongue disease that should be considered according to their experience of managing outbreaks in the field, to understand whether we were using the most appropriate environmental inputs to our risk models. We ascertained the time scale and geographical resolution (district, state, village level) at which forecasts and risk maps would be of maximum value to them and the means by which they would prefer them to be communicated. These insights will be extremely valuable for tailoring IBVNet forecasts and risk maps to stakeholder needs when these are delivered in early 2015.
Year(s) Of Engagement Activity 2014
URL http://www.IBVNet.com
 
Description UK-INDIA COLLABORATION ON BLUETONGUE RESEARCH 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? Yes
Geographic Reach International
Primary Audience Participants in your research or patient groups
Results and Impact BBSRC Impact case study on IBVNet project UK-INDIA COLLABORATION ON BLUETONGUE RESEARCH

no actual impacts realised to date
Year(s) Of Engagement Activity 2012
URL http://www.bbsrc.ac.uk/web/FILES/Publications/uk-india-bluetongue-research.pdf