Monitoring and Intervention Strategies for Bluetongue Virus Epidemics in Rural India

Lead Research Organisation: The Pirbright Institute
Department Name: UNLISTED

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 The project aim was to improve our understanding of bluetongue virus (BTV) transmission in India with a view to reducing the impact of this virus on sheep and particularly those animals kept by subsistence farmers. BTV is transmitted by Culicoides biting midges whose larvae develop in semi-aquatic habitats on farms and a major aspect of the project was to investigate populations of these vectors in detail across three southern India states (at the time the research was carried out, these were Tamil Nadu, Karnataka and Andhra Pradesh). All of these states experience monsoons that were thought to drive habitat creation for Culicoides larval development. Within the project we:

1) Characterised the Culicoides fauna seasonality in Southern India: We carried out insect trapping across the three states using standardised procedures and 30 widely distributed sites, the first time that this has been achieved in India. This included trials to choose the best trap to use, training local workers to carry out the trapping and then putting in place additional support to these sites. Initially we characterised the taxonomy of Culicoides populations selected from populations across southern India. We found that there were a series of potential vectors of BTV across this region and this led to a further meeting-based project funded by UKRI that brought together workers from across India to understand the implications of these studies. In parallel to this data collection we also conducted analyses on existing BTV distribution and seasonality maps that highlighted the role of buffalo as a host for BTV and which has been published in a peer reviewed article. Risk maps derived from this data and the Culicoides seasonality data are now being combined for a further publication.
2) Control techniques already in use by farmers in India to control BTV were also trialled for efficacy in killing Culicoides and were not demonstrated to have a clear impact. Not only are leaflets distributed to inform farmers inaccurate in identifying Culicoides breeding habitats (emphasising treatment of water bodies) but we also demonstrated emerging evidence of resistance to deltamethrin, a commonly used synthetic pyrethroid. Data from within the project is now being used to revise advise to farmers for practical application and emphasise the use of vaccination as a primary tool for disease control.
Exploitation Route We have created a framework for working on the India Culicoides fauna and also built models that can be used to predict future outbreaks of the virus. Linking directly to virus transmission in the field would provide a clearer understanding of how different vector-virus interactions might influence the impact of disease on farmers. Additionally, economic analysis of BTV impacts in the field in comparison to other viral diseases of livestock would be useful in prioritising responses.
Sectors Agriculture, Food and Drink,Communities and Social Services/Policy,Environment

URL https://bbsrc.ukri.org/documents/uk-india-bluetongue-research-pdf/
 
Description The project PhD student, Mudassar Chanda (MC), took study leave from his employment at Project Directorate on animal disease monitoring and surveillance (PD_ADMAS) in order to complete the PhD. He has enabled the project to forge new links with PD_ADMAS leading to improved access to both disease and meteorological datasets from India and knowledge exchange with epidemiologists in this organisation. In particular, we are in consultation to facilitate wider application of the modelling approaches (used to link variability in monsoon conditions, hosts and landscape to disease incidence) to other top ranking animal health diseases in India with a view to producing quantitative accessible risk maps and forecasts.
First Year Of Impact 2016
Sector Agriculture, Food and Drink
Impact Types Policy & public services

 
Description India Strategy Meeting
Geographic Reach Europe 
Policy Influence Type Influenced training of practitioners or researchers
Impact Meeting In India during 2014 with key policy makers to inform use of GIS in India to map BTV.
URL http://www.bbsrc.ac.uk/web/FILES/Publications/uk-india-bluetongue-research.pdf
 
Description GCRF Networks in Vector Ecology
Amount £1,035,634 (GBP)
Funding ID BB/R005362/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 07/2017 
End 06/2020
 
Description International Workshop: Reaching a consensus on Culicoides taxonomic identification in India
Amount £10,000 (GBP)
Funding ID BB/K021214/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 04/2013 
End 04/2014
 
Description 'Bluetongue and Culicoides in India'. Invited Lecture. Linnaean Society, London. Royal Entomological Society. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Scientific presentation to entomological audience.
Year(s) Of Engagement Activity 2011
 
Description Culicoides as vectors of arboviral disease. Carpenter, S. Invited speaker: LaLa Lajpat Rai University of Veterinary and Animal Sciences. 15/03/12. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Invited talk to University as part of project. Aimed at maintaining links to major collaborator.
Year(s) Of Engagement Activity 2012
 
Description International Congress of Entomology (Florida) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Chaired session and gave presentation on progress in Culicoides research. Largest ever meeting involving the Culicoides community with 100+ attendees.
Year(s) Of Engagement Activity 2016
URL http://ice2016orlando.org/
 
Description Public Health Entomology Group (LSHTM) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Invited lecture on 4th April 2017.
Year(s) Of Engagement Activity 2017
 
Description • 'Understanding bluetongue virus and Culicoides worldwide: a new India/UK collaboration' Tamil Nadu Veterinary University. Invited lecture. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presentation on Culicoides and BTV research to audience in India. Follow up discussion around project being run there and linked to scientists interested in the field.
Year(s) Of Engagement Activity 2011
URL http://www.ibvnet.co.uk