Spatial and temporal dynamics of AMR transmission from the outdoor environment to humans in urban and rural Bangladesh

Antibiotic resistant bacteria can be found in freshwater, soil, wastewater and among livestock. It is not yet known, however, how easily these resistant bacteria in the outdoor environment can be transmitted to humans. Research is needed on the human health risk from antimicrobial resistance (AMR) in the natural environment, and research is required in locations with high levels of AMR in the environment and where humans are at high risk of environmental exposure. Bangladesh is one such location where many factors favour the transmission of antibiotic resistance such as the widespread bacterial contamination of soil and drinking water; high human population densities; inadequate sanitation and poor treatment of wastewater alongside regular floods and natural disasters. Furthermore, inexpensive antibiotics are readily available from over-the-counter suppliers leading to widespread use in humans and animals.

This study will examine whether there is a health risk to humans from being exposed to AMR in the outdoor environment in Bangladesh. The novelty of the study is that it will measure the quantity of resistant bacteria in the outdoor environment (freshwater, soil, wastewater) and relate this to the presence of resistant bacteria in livestock (poultry) and humans at the same time and in the same locations. This will also be one of the first studies to measure AMR in humans with high and low exposure to contaminated environments.

The study will take place in three locations where transmission is likely to be high because of human interaction with animal and environmental reservoirs of AMR contamination. These locations are urban markets selling live poultry in Dhaka city, commercial poultry farms and rural villages where poultry and humans share living and sleeping areas.

We will measure the quantity of resistant bacteria in the gut (faeces) of humans who live or work closely with poultry (such as live poultry sellers and slaughterers, commercial poultry farm workers and village women who have poultry living in the household). These rates will be compared to humans who share similar environments but have little or no exposure to poultry. We predict that the resistant bacteria from the gut of chickens will be present in poultry faeces and that this is a potential route of AMR transmission to humans through close contact. We also predict that there will be more AMR bacteria in poultry that are given antibiotics regularly in poultry feed or as medication and this will increase the risk of AMR bacteria in humans.

A further aim is to study how resistant bacteria in the environment change over time by comparing the quantity of resistant genes in water, soil and waste during the dry season and wet season in Bangladesh. Understanding the seasonal changes of AMR in the outdoor environment will enable us to target interventions at times when the risks of transmission of AMR are highest.

Finally, we will examine the cultural and social practices in animal husbandry and poultry keeping in relation to the use of antibiotics as medicine and in animal feed. We will observe the practices of farm workers, slaughterers and market sellers to assess which aspects of food production, selling and disposal of poultry waste contaminate the environment, and what human activities (hand washing, use of gloves, handling of poultry) increase or decrease risk of exposure to AMR. We will use this information to identify ways of reducing the spread of AMR among animals and humans.

This study will provide new insight into whether AMR in the environment is a serious threat to human health. As new forms of resistant genes and bacteria are spreading rapidly in south Asia, there is an urgent need to establish how AMR can be transmitted through water, soil, waste and livestock, and identify what can be done to reduce this transmission at a global level.

The impact of our research will be to bring about improvements in environmental quality and global public health. This will be done through mobilisation of stakeholders, beneficiaries and users of the knowledge gained on AMR in the outdoor environment.
The beneficiaries of this research include:
1. Participating groups with high exposure to AMR in the environment in Bangladesh, such as members of the Dhaka Market Association, live poultry sellers, slaughterers, municipal waste collectors, poultry farm workers, village women.
2. Commercial and private enterprises in Bangladesh such as Dhaka city municipality with responsibility for food and live poultry markets; the Market Association Heads in Dhaka city and commercial poultry farm owners.
3. Ministries and local government workers in Bangladesh: including the Ministry of Health and Family Welfare; Livestock and Fisheries and the Ministry for Local Government. Local government workers include the government veterinary officers with responsibility for commercial poultry farms, and local district workers responsible for environmental health.
4. International policy makers, donors and advisory groups such as the Department for International Development; the Food and Agriculture Organisation, and the WHO advisory group on Integrated Surveillance of Antimicrobial Resistance (WHO-AGISAR). UK AMR stakeholders also include the advisory board members of the AMR Bridging the Gaps network at Loughborough University (EP/M027341/1) drawn from industry, clinical practice and learned societies. We also seek to work with Public Health England, the Food Standards Agency to exchange knowledge and apply relevant findings to UK settings.

Local stakeholders will benefit from regular engagement in the research process through consultation with the investigators at the beginning, middle and end of the project. The ministerial and international stakeholders are likely to benefit at the later stages of the project when findings are translated into materials for dissemination and impact activities.
The priorities of local stakeholders will be sought at the outset of the project regarding animal husbandry practices and food production for live birds/poultry; solid and liquid waste management in commercial farms and urban markets, and the interactions between national and local government with local pharmacies and private practitioners who prescribe antibiotics for humans and animals. The consultations during this stage will also inform the research planning, particularly the study questionnaire tool and ethnographic research.

Potential benefits of the research
The stakeholders and users of this research will benefit from greater knowledge on the potential for AMR transmission from the outdoor environment to humans. Further benefits will be gained from establishing whether occupational exposure to sources of AMR poses a significant risk to human health. These findings will be used to develop policy briefings or proposals to effect change that will improve environmental quality and improve global public health. Potential scenarios of change are: reduced environmental contamination (e.g. improved water quality; reductions in sources of AMR contamination); building a community of practice (e.g. design solutions and innovation in food production, waste disposal), or translation to policy. Implementation of change would be an area for development after the lifetime of the project through follow-on funding proposals. Government bodies will benefit from robust data from non-clinical samples (rural and urban) on which to assess the scale and spread of antimicrobial resistant bacteria in humans, poultry and in the outdoor environment in Bangladesh. This will enable mapping of changes over time and, in the absence of routine surveillance of AMR in Bangladesh, will provide important baseline data on which to formulate policies or implement surveillance programmes.