Chicken or Egg: Drivers for Antimicrobial Resistance in Poultry in India (DARPI)

Lead Research Organisation: University of Liverpool
Department Name: Institute of Infection and Global Health

Abstract

The aim of this study is to first to map antimicrobial use (AMU) and the antimicrobial resistance (AMR) that is driven by inappropriate use, across the entire poultry meat supply chain from farm to table in India. The study provides [1] a unique opportunity to map AMU, [2] to understand entry points for development of AMR and [3] the contribution by inappropriate AMU in poultry, and [4] suggests potential solutions to address the huge AMR burden in India.
AMR is a major global health risk, particularly in developing countries, threatening human and animal health. Contributing to this problem is the inappropriate use of antimicrobials in people and livestock production. India has a high burden of infectious disease, and bacteria from human clinical infections are becoming increasingly difficult to treat, with fewer treatment options available. Studies suggest that livestock may commonly carry resistant bacteria in their gut, with poultry and poultry meat also identified as a source of such bacteria. However, there is a complete lack of data on the scale of the problem, or on what antimicrobials are being used in poultry meat production, how they are used, and how this contributes to the carriage of AMR bacteria that may be a threat to human and animal health.
Poultry meat is one of the main protein sources in Indian and is the fastest growing livestock sector. Increasingly, poultry meat in India is produced through more intensive integrated or semi-integrated farming systems where antimicrobials are used for various purposes, including for growth promotion, to prevent and treat disease. To date there have been no comprehensive studies on AMU or AMR through the poultry meat supply chain. Our interdisciplinary project aims to address these data gaps by studying the poultry meat food supply in its entirety to determine: behaviours that drive AMU and how these contribute to the selection and transmission of AMR, to inform better use; to design with farmers and other stakeholders interventions to reduce AMU/AMR, which are cost-effective and easy to implement; determine the economic impact from changing AMU practices, or using alternatives. The project will involve working closely with the poultry industry, policy makers and other stakeholders throughout to ensure the findings have impact.
This project is timely in providing crucial data to inform antimicrobial stewardship: the trajectory of the Indian poultry industry is shifting towards intensive farming and AMU is predicted to rise substantially. Therefore, this is an opportunity to intervene through working closely with stakeholders to provide alternative strategies for sustainable AMU. The project also offers other benefits, with a strong social science component providing unique insights into behaviours driving AMU, as well as service design enabling visualization of AMU and AMR, and co-design strategies. Indian researchers will be trained in these methods, building capacity for social science in Indian agricultural and veterinary research that will have value long after the conclusion of this project.
The study will be the first to map AMU and AMR in the entire poultry meat supply chain from farm to table in India. The study provides a unique opportunity to map AMU, understand entry points for development of AMR and the contribution by inappropriate AMU in poultry, and suggest potential solutions to address the huge AMR burden in India.

Planned Impact

DARPI is a strong interdisciplinary team using a systems approach to tackle the important issue of AMR in the Indian poultry meat industry. Communicating with the Indian poultry industry and other stakeholders, through partnerships, workshops, industry events, social media, newsletters and publications is central to our ambitious research programme. Ultimately we aim to identify drivers of AMU and AMR to facilitate rationale prescribing, through education, training and alternative strategies, to reduce the burden of AMR in the poultry food production chain, to the benefit of both animal and public health.
Social and economic
The project will enhance understanding of the business practices and processes that underpin the current flow of antimicrobials through the poultry supply chain in India and how this is changing with increasing intensification, in line with predicted future trajectories. The current flow of antimicrobials will be characterised by drivers and inhibitors of use, including awareness and understanding of antimicrobials and AMR amongst poultry workers; level of education and training around prescribing; and risk perceptions around potential or perceived changes to current AMU.
Beneficiaries:
Indian research institutes by introducing and training in, social science and design research methodologies to enable a cross-disciplinary approach to the challenges of AMR, in particular by building a better understanding of everyday AMU that is essential for implementing more rational stewardship of antibiotics through the poultry supply chain.
Indian poultry farms by creating a clear mapping of the flow of antimicrobials into the poultry supply chain, to visualise and identify where drivers of AMR are strongest and what processes may lead to more rational AMU at key points along the supply chain. In addition, applying a bottom up approach, through co-design with end users to articulate and communicate good practice to farmers.
The Indian poultry industry: by enhancing understanding of drivers and motivations; and the processes and procedures that enhance or inhibit more rational use of antimicrobials at key points along the poultry supply chain by farm workers and animal health workers. Such data will inform guidelines and training across the industry to improve practices and communicate best practice for AMR minimization. The co-design of interventions with industry will ensure that such interventions are feasible, acceptable and cost-effective. Furthermore, these tools will be developed with consideration of the future industry trajectory, so that approaches are scalable and sustainable and able to react to accommodate anticipated trajectory development.
The Indian veterinary industry by mapping how AMU along the poultry supply chain is understood and initiated by farm workers, managers and animal health workers and whether current usage patterns may drive AMR in poultry and humans. In addition, this work will highlight where further education and training is required on antimicrobial prescribing, with a MOOC will be developed to cover such gaps.
The Indian pharmaceutical industry by improving understanding of how inappropriate use of antimicrobials in the poultry supply chain may drive AMR, so that promotion of antimicrobials, information and guidelines for use can be rationalised to minimise the emergence and spread of resistance.
The Indian media by enhancing understanding of AMU in the poultry industry its contribution to the emergence and spread of resistance will support more scientifically accurate and appropriate solutions to highlight and tackle the existing problem.
The Indian policy community to will inform clear briefing papers on the link between poultry industry practices and the emergence and spread of AMR, with economic comparisons of alternatives. Our findings will inform the Indian NAP on AMR, highlighting pathways to behaviour change and where regulatory/policy frameworks are inadequate.

Publications

10 25 50

 
Description Determining the drivers for Antimicrobial Use (AMU) & defining the socio-economic context of AMU: Interviews with key stakeholders along the poultry value chain in three states of southern India (Tamil Nadu, Karnataka, and Telangana) indicated wide use of antimicrobials as therapeutic and prophylactic agents. In addition, the Indian poultry industry is dominated by a few integrators who control production, as they are the main financial and technical suppliers. Integrators, farm supervisors, and veterinarians are key actors in controlling AMU on broiler farms. Antibiotic alternatives such as probiotics, prebiotics, bacteriophages and immunostimulants are available, however, quality control and regulations for production and marketing is less stringent compared to pharmaceuticals. Furthermore, there is little data available to support their efficacy. Therefore, further data is required on their entry points into poultry production and monitoring of their effectiveness.
Co-design of interventions: Whilst the co-design of interventions has been hindered by the pandemic, a disease control map was developed with stakeholders. This revealed biosecurity measures, as a preferred disease control solution, do not currently reflect the lived realities of many stakeholders working on farms. The evidence produced from applying the disease control map indicates that terms such as biosecurity, often promote a farming system that is defined by veterinarians, scientists, and integrators who have international co-operations in, or exposure to the Global North.
As with other complex systems, the poultry supply chain, has the potential to manifest into a hegemonic structure in which specific types of knowledge and certain practices come to have more value than others. As a result, researchers should find ways in which to involve different stakeholders in the co-design process, as a way of co-creating value and initiating more equitable and sustainable practices.

Defining AMR at key points in the system and optimising antimicrobial use: Moderate to high levels of 3rd generation cephalosporin resistant multi-drug resistant (MDR) E. coli have been found in Indian poultry farms and their external environment, as well as in hatcheries, suggesting multiple points for entry into the poultry value chain.
In addition, antibiotic residues, including above the maximum residue levels for chlortetracycline have been found in retail chicken meat across the three states. However, interviews with some actors suggest that administration may be occurring post-farm to improve bird condition prior to sale within wholesale markets and which requires further exploration.
With regards to antimicrobial growth promoters (AGP), five AGPs (virginiamycin, chlortetracycline, bacitracin methyl disalicylate, lincomycin and tylosin) were investigated for their impact on performance variables and AMR using culture independent approaches. No significant effect of AGPs were found on cumulative growth or feed efficiency parameters at the end of the production and or mortality rates. In addition, antibiotic resistance genes (ARGs) were ubiquitous in the chicken gastrointestinal tract irrespective of AGP supplementation. These results suggest that AGPs do not have a major influence on growth parameters or ARG carriage.
Broiler infection experiments with a 3rd generation cephalosporin resistant MDR E. coli demonstrated spread from seeder birds to all birds within a group within 7 days. Treatment with the antibiotic amoxicillin promoted greater persistence of the resistant E. coli in birds up to 35 days of age. Interestingly, regardless of treatment, resistance to further antibiotic classes emerged in the infecting strain, including to fluoroquinolones, despite no exposure to this drug. Further work also examined the impact of commercial coccidiostats, which are common poultry feed additives worldwide to prevent coccidiosis, which can impact poultry gut health. Significantly increased AMR in E. coli to b-lactam drugs including to cephalosporins was observed in the treated group. Whilst one component of the coccidiostat is known to have antibacterial properties, these not directed at E. coli. Further investigation is required to elucidate the mechanism promoting AMR, which may be related to changes in microbial communities.
Exploitation Route The findings from this study informs on who the key actors are concerning antimicrobial use in Indian broiler production and who should be targeted around education or policy changes concerning antimicrobial stewardship for policy makers and integrated poultry production companies. Furthermore, our current work on undergraduate veterinary education concerning antimicrobial stewardship and AMR should be of benefit to the academic community around curriculum gaps within veterinary degress curriculum and inform on areas for continuing professional development programmes.
The presence of antibiotic residues in meat is also important for regulators and ensuring that regulation is sufficient to ensure that antimicrobial withdrawal periods are adhered to, including when the birds leave the farm and are sold as live birds and kept before slaughter.
The findings around antimicrobial growth promoters demonstrate that the use of these does not significantly improve production, which is of value to poultry producers and their reliance on such feed additives which are not cost neutral.
Sectors Agriculture, Food and Drink,Education,Government, Democracy and Justice

 
Description Global Burden of Animal Diseases framework
Amount $900,000 (USD)
Organisation Bill and Melinda Gates Foundation 
Sector Charity/Non Profit
Country United States
Start 09/2017 
End 12/2021
 
Description Global Burden of Animal Diseases programme
Amount $7,000,000 (USD)
Organisation Bill and Melinda Gates Foundation 
Sector Charity/Non Profit
Country United States
Start 01/2021 
End 12/2022
 
Description Global Burden of Animal Diseases Programme 
Organisation Commonwealth Scientific and Industrial Research Organisation
Department CSIRO North Ryde
Country Australia 
Sector Public 
PI Contribution Jonathan Rushton has led the development of the Global Burden of Animal Diseases programme. An initiation of this programme was published in 2018 and a rollout in 2021,
Collaborator Contribution Mario Herrero and his team (CSIRO) lead the work on Populations and Production systems. Mieghan Bruce (Murdoch University) lead the work on Ontology and Attribution Delia Grace and her team (ILRI) lead the Disease Prioritisation work Barbara Wieland and Theo Knight-Jones (ILRI) lead the country case study for Ethiopia They have also led the development of a concept note for a case study in Indonesia
Impact Funded rollout proposal from BMGF and FCDO Funded cases study from ACIAR Comments in the Lancet 2018 and 2020
Start Year 2018
 
Description Global Burden of Animal Diseases Programme 
Organisation International Livestock Research Institute (ILRI)
Country Kenya 
Sector Charity/Non Profit 
PI Contribution Jonathan Rushton has led the development of the Global Burden of Animal Diseases programme. An initiation of this programme was published in 2018 and a rollout in 2021,
Collaborator Contribution Mario Herrero and his team (CSIRO) lead the work on Populations and Production systems. Mieghan Bruce (Murdoch University) lead the work on Ontology and Attribution Delia Grace and her team (ILRI) lead the Disease Prioritisation work Barbara Wieland and Theo Knight-Jones (ILRI) lead the country case study for Ethiopia They have also led the development of a concept note for a case study in Indonesia
Impact Funded rollout proposal from BMGF and FCDO Funded cases study from ACIAR Comments in the Lancet 2018 and 2020
Start Year 2018
 
Description Global Burden of Animal Diseases Programme 
Organisation Murdoch University
Country Australia 
Sector Academic/University 
PI Contribution Jonathan Rushton has led the development of the Global Burden of Animal Diseases programme. An initiation of this programme was published in 2018 and a rollout in 2021,
Collaborator Contribution Mario Herrero and his team (CSIRO) lead the work on Populations and Production systems. Mieghan Bruce (Murdoch University) lead the work on Ontology and Attribution Delia Grace and her team (ILRI) lead the Disease Prioritisation work Barbara Wieland and Theo Knight-Jones (ILRI) lead the country case study for Ethiopia They have also led the development of a concept note for a case study in Indonesia
Impact Funded rollout proposal from BMGF and FCDO Funded cases study from ACIAR Comments in the Lancet 2018 and 2020
Start Year 2018
 
Description "Drivers of antimicrobial resistance in poultry in India: chicken or egg?" (oral presentation at a veterinary conference). 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Invited speaker at the 7th Pan-Commonwealth Veterinary Conference, Bangalore, India, 2019 (oral presentation) by Dr Nag Hegde, Indian PI. Introduced the audience to the project and interdisciplinary approach and challenges around AMR.
Year(s) Of Engagement Activity 2019
 
Description "Incorporation of social science to AMR projects - value added, any lessons learnt." short presentation. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact India-UK Antimicrobial Resistance Workshop, Delhi, India, 2019. Presentation given by the Indian PI to a AMR workshop consisting of Indian and UK academic delegates.
Year(s) Of Engagement Activity 2019
 
Description 4. NR Hegde. Oral presentation on "Antimicrobial resistance: chicken or egg?" at a conference. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Presentation at the Annual Conference of the Association of Microbiologists of India, and International Symposium on Host-Pathogen Interactions, Hyderabad, India, 2018.
Year(s) Of Engagement Activity 2019
 
Description AMR masterclass in Nairobi, Kenya. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Professor Williams taught on a AMR masterclass around diagnostics of AMR which included a practical class and DARPI presented as a case study around methodology to delegates (~27) from Kenya, Ethiopia, Eritrea, Somaliland and Somalia. The attendees included junior and more senior academics and both undergraduate and postgraduate students who attended this two day masterclass as part of the One Health in the Horn of Africa GCRF project. Attendees have since contacted Professor Williams who is advising on protocols for research and diagnostics by some of the delegates and who wish to collaborate.
Year(s) Of Engagement Activity 2019
 
Description Causing a Flap: chicken-based research to inform industry, education & human well-being engagement day, 28th August, Woburn House London. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Other audiences
Results and Impact Invited speaker at this interdisciplinary event to talk about the challenge of controlling antimicrobial use and antimicrobial resistance in the poultry industry in the UK and India.
~50 people were present from diverse disciplines, including the history, archeology and the arts. This was a really useful event to attend and speak at in terms of the different methods used in the Causing a Flap project for public engagement in the UK and overseas, as well as bringing biological context to modern issues in intensive poultry production, which sparked lots of debate.
Year(s) Of Engagement Activity 2019
URL https://www.eventbrite.co.uk/e/causing-a-flap-chickens-in-industry-education-human-well-being-ticket...
 
Description Discussions with CSIRO on the Global Burden of Animal Diseases programme 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Meeting was held with senior management of CSIRO on their potential contributions to the Global Burden of Animal Diseases programme. They subsequently contributed to a successful proposal for the rollout of the GBADs programme that is funded by the Bill and Melinda Gates Foundation and FCDO. They also contributed to the development of a successful concept note for case study work in Indonesia funded by ACIAR.
Year(s) Of Engagement Activity 2020
 
Description ISID/ProMED conference Invited Talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Dr Jenni Cole (RHUL) was Invited to talk at a international conference (ISID/PROMED) on the integration of social science in AMR research with DARPI used as the exemplar.
Consisted of a multi-disciplinary audience of academics and others.
Year(s) Of Engagement Activity 2018
 
Description Invited presentation at the ACIAR funded workshop on African Swine Fever. The talk was about the impact of animal diseases and the Global Burden of Animal Diseases programme 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Workshop was organised to discuss ongoing research on the outbreaks of ASF in Asia. Reports were made from different countries and Jonathan Rushton made a presentation on the Global Burden of Animal Diseases programme. Following this meeting ACIAR have worked with the GBADs programme in developing a concept note for funding with activities in Indonesia.
Year(s) Of Engagement Activity 2020
URL https://aciar.gov.au/media-search/news/disease-experts-meet-canberra
 
Description Invited speaker at OIE 2nd AMR Meeting in Marrakech, Morocco. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Professor Jonathan Rushton was invited to speak at the OIE 2nd AMR Meeting in Marrakech, October 2019.
The presentation was on the use of economics for selection interventions and policies, with particular reference to tackling AMR through reduced antimicrobial use.
It was attended by Government veterinary services, private sector (Pharmaceutical companies, livestock companies, food system representatives) and international organisations plus some University academics.
Year(s) Of Engagement Activity 2018
URL http://www.oie.int/amr2018/en/
 
Description One Health workshop on antimicrobial use and resistance 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact A two day workshop on antimicrobial use and resistance was ran for participants in Kenya, but included post-grad students and practioners from Kenya and Ethiopia.
This introduced students to some of the methods and approaches used in DARPI and enabled the students to explore the issues around AMU and AMR. Feedback on the workshop were extremely positive in helping participants think about the situation in their own countires and their research.
Year(s) Of Engagement Activity 2019
 
Description Online One Health workshop on AMR and Antimicrobial use (AMU) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact A four day workshop was ran online for participants in Kenya, Ethiopia, Eritrea and Somaliland on AMR and AMU and which introduced participants to issues around AMR and AMU from a One Health perspective and methodologies and approaches used within DARPI.
Feedback was extremely positive from participants and NJ Williams has been contacted for further support around development of AMR activities.
Year(s) Of Engagement Activity 2021
 
Description Poster presented at the India International Science Festival, Lucknow, India, 2018. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Schools
Results and Impact Poster presentation at public science festival and work on the project discussed with attendees.
Year(s) Of Engagement Activity 2019
 
Description Presentation about Campylobacter control at the 7th Pan Commonwealth Veterinary Conference, Bangalore March 2019 
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 on the infection biology and control of Campylobacter in broilers and the broiler meat chain.
~70 people attended from India and other commonwealth countries
Year(s) Of Engagement Activity 2019
 
Description Presentation of the Global Burden of Animal Diseases programme to an academic and industry meeting 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact A meeting was organised by Murdoch University, Perth, Australia to discuss the Global Burden of Animal Diseases programme with academics in the veterinary faculty, Western Australia veterinary services with the CVO present and the pharmaceutical industry. Resulting from the meeting was a successful application of support for GBADs from the Bill and Melinda Gates Foundation and FCDO with Murdoch as a partner of an international consortium and Dr Mieghan Bruce as a theme lead
Year(s) Of Engagement Activity 2020
URL https://www.murdoch.edu.au/news/articles/taking-a-one-health-approach-to-animal-diseases
 
Description Social Science for Scientists Summer School 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact 30 researchers, postgraduate students, PhD students and research assistants, most of whom were microbiologists, veterinary scientists, animal nutrition specialists and from other scientific disciplines, attended a five day summer school where they learned basic social science field techniques including interview skills, observational skills, transect walks, mapping, service design, participatory rural action (PRA) and ethics. The week included one day's practical training in the field.

The training provided the scientists with basic skills that will enable them to collect some social science data alongside microbiological sampling on farms, thus increasingly the social science capacity of the project.
Year(s) Of Engagement Activity 2019
 
Description Stand at Poultry India, November 2018. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact We hosted a stand at Poultry India which is attended by industry from India and neighbouring countries, as well as global industry players.
We used the stand to promote the project and interact with stakeholders, and make them aware of the project and discuss the issues they have around AMR.
We were informed about issues that vets are facing in treating infections due to AMR and we had requests from farmers (including those based outside of India) to engage them in our research.
Year(s) Of Engagement Activity 2018
 
Description Stand at Poultry India, November 2019. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact We held a stand at Poultry India to interact with the poultry industry and other stakeholders, and used a number of methods to obtain the views and priorities of those attending this industry fair. We were able to talk to farmers who work in different regions who have different issues and are managing a range of different types of farms, or are supplying products to the industry. The stand generated a lot of interest in AMR, not just from a disease perspective and managing this on poultry farms but individuals indicated they were concerned about the risk of AMR to their own and their families health, which is something we had not encountered before from those working in the industry and which can be explored more. We also made a number of contacts who are interested in being involved in our research.
Year(s) Of Engagement Activity 2019
 
Description World Veterinary Poultry Association (India) Conference 2020 (ICAR-National Institute of animal Nutrition and Physiology) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Potential innovations in poultry industry particularly vaccines, diagnostics and nutrition.
Year(s) Of Engagement Activity 2020
URL http://www.wvpaindiaconference.com/