Human exposure to antimicrobial resistance from poultry production: Assessing hygiene and waste-disposal practices in Bangladesh

doi:10.1016/j.ijheh.2019.07.007

International Journal of Hygiene and Environmental Health

Volume 222, Issue 8, September 2019, Pages 1068-1076

https://doi.org/10.1016/j.ijheh.2019.07.007 Get rights and content

Abstract

The unregulated use of antibiotics is linked with intensive poultry farming in developing economies. In low-and middle-income countries, the dissemination of antimicrobial resistance (AMR) has also been attributed to contamination, poor public health infrastructure and inadequate waste disposal practices. There are limited data on hygiene and waste disposal practices in small-scale commercial and household poultry farming and market sales in Bangladesh. Our objective was to explore human exposures, hygiene and waste disposal practices in poultry raising and processing to identify probable pathways for transmission of AMR bacteria.

We employed mixed methods approaches of in-depth interviews and structured observations to assess exposures, hygiene behaviours and waste-disposal practices relating to poultry production in Bangladesh. Interviews (n = 18) were conducted with commercial poultry farmers, backyard poultry owners, and live poultry market workers. Structured observations were conducted for 6-h in five households, five commercial farms and five urban live bird markets to assess the frequency of transmission/exposure events in these settings.

Interviews highlighted existing practices that can contribute to transmission of antimicrobial resistant bacteria from poultry to humans. In households and farms, untreated poultry waste and carcasses were disposed of on agricultural fields and in water bodies which may contaminate surface water and soil with poultry faeces. Biosecurity precautions were not used, and hands were rarely washed with soap after handling poultry. In urban markets, live poultry slaughter and processing was done on site with bare hands which were subsequently rinsed in water stored in containers without soap. Solid waste from poultry processing was disposed into municipal waste disposal stations and liquid waste was discarded into open drains.

Structured observations revealed that workers in live poultry markets had the highest direct contact with poultry and poultry waste, almost tenfold higher than those working in poultry farms or with domestic poultry (59 vs 544 observed direct poultry exposure events) placing them at particularly high risk of exposure to faecal bacteria. Biosecurity measures were limited; in some cases, workers in commercial farms and urban markets had gloves and masks but often did not use them. In 88% (606/689) of exposure events no handwashing took place. Eating and drinking after handling poultry and without washing hands was observed in all three settings. These data suggest effective intervention strategies to reduce environmental contamination and to decrease risks of transmission should be prioritized. Data on prevalence of risk behaviours and AMR transmission to humans along environmental pathways can inform policy and intervention strategies.

Section snippets

Background

The requirement for animal-sourced protein for human consumption is increasing globally at an unprecedented rate (Van Boeckel et al., 2015). To meet this demand, production techniques for livestock and poultry rearing strives for increasing cost-effectiveness (Silva et al., 2013; Zhu et al., 2013). In Bangladesh, the poultry sector accounts for 14% of the total value of livestock output. Poultry meat alone contributes 37% of the total meat production in Bangladesh (World's Poultry Science

Methods

To determine poultry raising practices, poultry handling and waste disposal practices, we selected three groups with differing human-poultry interactions in order to assess the potential routes of AMR bacteria transmission in each setting: 1) rural villages where they use traditional animal husbandry, who usually raise less than 20 poultry (Chowdhury, 2013), 2) small and medium-size commercial poultry farms in peri-urban sites around Dhaka (small farms typically have 500–1000 poultry; medium

Backyard poultry

Respondents were all female, aged 21–40 years and had been rearing poultry for the last 4–30 years. Poultry, especially chickens were predominantly reared for eggs and occasionally for meat. Chickens were not kept in pens or sheds during the day but roamed around the households and courtyards. Participants, when asked whether they handled poultry during day to day care reported that usually direct poultry handling was only required when slaughtering or separating ill birds from the rest of the

Discussion

Rural poultry owners, workers in small to medium scale commercial poultry farms, and workers and waste collectors in urban live bird markets demonstrated behaviours leading to direct exposure to poultry faeces through handling, slaughtering and processing without the use of protective equipment.

Our structured observation revealed that rural households had the lowest frequency of direct exposure to poultry, commercial farmers had intermediate frequency of exposure, and market live poultry

Conclusion

To our knowledge, this is the first study to use structured observations to compare relative frequency of potential AMR bacterial transmission and exposure events between humans and poultry in resource-poor settings. We have not seen any previous study that has related known animal exposures to likelihood of transmission of resistant bacteria from poultry to humans, but this is a first step in identifying the key behaviours and understanding exposures. A further strength of the study is taking

Author's contribution

Mahbub-Ul Alam, MPH, Mahbubur Rahman, MSPH, Abdullah-Al-Masud, MPH, Mohammad Aminul Islam, PhD, Md. Muhammad Asaduzzaman, MPhil, Supta Sarker, MSc, Emily Rousham, PhD, Leanne Unicomb, PhD.

Contributors: ER, MAI, and LU conceived and designed the original protocol. All authors were involved in designing the data collection instrument, and selection of field sites. Data entry, cleaning and analysis was carried out by AAM, SS, and MA. ER, LU, and MAI provided advice on data interpretation and

Acknowledgement

This work was supported by the Natural Environment Research Council, UK, under the Antimicrobial Resistance Cross Council Initiative supported by the seven UK research councils (Award number: NE/N019555/1). icddr,b is thankful to the Governments of Bangladesh, Canada, Sweden and the UK for providing core/unrestricted support. Authors would like to thank participants and data collectors of the study.

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¹: Contributed equally to the first author.

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Human exposure to antimicrobial resistance from poultry production: Assessing hygiene and waste-disposal practices in Bangladesh

Abstract

Section snippets

Background

Methods

Backyard poultry

Discussion

Conclusion

Author's contribution

Acknowledgement

Lancet Planet Health

Am. J. Infect. Contr.

Environ. Res.

J. Dairy Sci.

Menstrual hygiene management among Bangladeshi adolescent schoolgirls and risk factors affecting school absence: results from a crosssectional survey

BMJ Open

Prospects of poultry industry in Bangladesh

Comparing the performance of indicators of hand-washing practices in rural Indian households

Trop. Med. Int. Health

Distribution, numbers, and diversity of ESBL-producing E. coli in the poultry farm environment

PLoS One

Antibiotic resistance in animal and environmental samples associated with small-scale poultry farming in Northwestern Ecuador

mSphere

The prevalence of extended-spectrum beta-lactamase-producing multidrug-resistant Escherichia coli in poultry chickens and variation according to farming practices in Punjab, India

Environ. Health Perspect.

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World's Poult. Sci. J.

Antimicrobial resistance in Escherichia coli isolated in wastewater and sludge from poultry slaughterhouse wastewater plants

J. Environ. Health

Structured observations of hygiene behaviours in Burkina Faso: validity, variability, and utility

Bull. World Health Organ.

Risk factors for human infection with avian influenza A H5N1, Vietnam, 2004

Emerg. Infect. Dis.

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Observed hand cleanliness and other measures of handwashing behavior in rural Bangladesh

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Avian Dis.

Dynamics and genetics of a disease-driven species decline to near extinction: lessons for conservation

Sci. Rep.

Poultry feather waste management and effects on plant growth

Int. J. Recycl. Org. Waste Agric.

A review of antibiotic use in food animals: perspective, policy, and potential

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PLoS Med.

Measuring hygiene practices: a comparison of questionnaires with direct observations in rural Zaire

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