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Global trends in antimicrobial resistance in animals in low- and middle-income countries
Livestock antibiotic resistance
Most antibiotic use is for livestock, and it is growing with the increase in global demand for meat. It is unclear what the increase in demand for antibiotics means for the occurrence of drug resistance in animals and risk to humans. Van Boeckel et al. describe the global burden of antimicrobial resistance in animals on the basis of systematic reviews over the past 20 years (see the Perspective by Moore). There is a clear increase in the number of resistant bacterial strains occurring in chickens and pigs. The current study provides a much-needed baseline model for low- and middle-income countries and provides a “one health” perspective to which future data can be added.
Structured Abstract
INTRODUCTION
The global scale-up in demand for animal protein is the most notable dietary trend of our time. Since 2000, meat production has plateaued in high-income countries but has grown by 68%, 64%, and 40% in Asia, Africa, and South America, respectively. The transition to high-protein diets in low- and middle-income countries (LMICs) has been facilitated by the global expansion of intensive animal production systems in which antimicrobials are used routinely to maintain health and productivity. Globally, 73% of all antimicrobials sold on Earth are used in animals raised for food. A growing body of evidence has linked this practice with the rise of antimicrobial-resistant infections, not just in animals but also in humans. Beyond potentially serious consequences for public health, the reliance on antimicrobials to meet demand for animal protein is a likely threat to the sustainability of the livestock industry, and thus to the livelihood of farmers around the world.
RATIONALE
In LMICs, trends in antimicrobial resistance (AMR) in animals are poorly documented. In the absence of systematic surveillance systems, point prevalence surveys represent a largely untapped source of information to map trends in AMR in animals. We use geospatial models to produce global maps of AMR in LMICs and give policy-makers—or a future international panel—a baseline for monitoring AMR levels in animals and target interventions in the regions most affected by the rise of resistance.
RESULTS
We identified 901 point prevalence surveys from LMICs reporting AMR rates in animals for common indicator pathogens: Escherichia coli, Campylobacter spp., nontyphoidal Salmonella spp., and Staphylococcus aureus. From 2000 to 2018, the proportion of antimicrobial compounds with resistance higher than 50% (P50) increased from 0.15 to 0.41 in chickens and from 0.13 to 0.34 in pigs and plateaued between 0.12 and 0.23 in cattle. Global maps of AMR (available at resistancebank.org) show hotspots of resistance in northeastern India, northeastern China, northern Pakistan, Iran, eastern Turkey, the south coast of Brazil, Egypt, the Red River delta in Vietnam, and the areas surrounding Mexico City and Johannesburg. Areas where resistance is just starting to emerge are Kenya, Morocco, Uruguay, southern Brazil, central India, and southern China. Uncertainty in our predictions was greatest in the Andes, the Amazon region, West and Central Africa, the Tibetan plateau, Myanmar, and Indonesia. Dense geographical coverage of point prevalence surveys did not systematically correlate with the presence of hotspots of AMR, such as in Ethiopia, Thailand, Chhattisgarh (India), and Rio Grande do Sul (Brazil). The highest resistance rates were observed with the most commonly used classes of antimicrobials in animal production: tetracyclines, sulfonamides, and penicillins.
CONCLUSION
The portfolio of antimicrobials used to raise animals for food is rapidly getting depleted, with important consequences for animal health, farmers’ livelihoods, and potentially for human health. Regions affected by the highest levels of AMR should take immediate actions to preserve the efficacy of antimicrobials that are essential in human medicine by restricting their use in animal production. In some middle-income countries, particularly in South America, surveillance must be scaled up to match that of low-income African countries that are currently outperforming them despite more limited resources. Policy-makers coordinating the international response to AMR may consider sparing African countries from the most aggressive measures to restrict access to veterinary drugs, which may undermine livestock-based economic development and rightfully be perceived as unfair. However, in regions where resistance is starting to emerge, there is a window of opportunity to limit the rise of resistance by encouraging a transition to sustainable animal farming practices. High-income countries, where antimicrobials have been used on farms since the 1950s, should support this transition—for example, through a global fund to subsidize improvement in farm-level biosafety and biosecurity.
Animals raised for food use the majority of antimicrobials sold on Earth.
The main article presents a map of antimicrobial resistance in animals in low- and middle-income countries where sales of veterinary antimicrobials remain largely unregulated. In this image, broilers are seen roaming freely outside of a family-owned farm in Kitwe, Zambia. [Photo: S. Jetha]
Abstract
The global scale-up in demand for animal protein is the most notable dietary trend of our time. Antimicrobial consumption in animals is threefold that of humans and has enabled large-scale animal protein production. The consequences for the development of antimicrobial resistance in animals have received comparatively less attention than in humans. We analyzed 901 point prevalence surveys of pathogens in developing countries to map resistance in animals. China and India represented the largest hotspots of resistance, with new hotspots emerging in Brazil and Kenya. From 2000 to 2018, the proportion of antimicrobials showing resistance above 50% increased from 0.15 to 0.41 in chickens and from 0.13 to 0.34 in pigs. Escalating resistance in animals is anticipated to have important consequences for animal health and, eventually, for human health.
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Science
Volume 365 | Issue 6459
20 September 2019
20 September 2019
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Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
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Received: 29 November 2018
Resubmitted: 19 April 2019
Accepted: 31 July 2019
Published in print: 20 September 2019
Acknowledgments
We thank J. Bastin for providing vegetation layers, S. Droz and V. Perreten for providing CLSI guidelines, and S. Nussbaumer for research assistance. Funding: T.P.V.B., C.Z., and N.G.C. were supported by The Branco Weiss Fellowship and the Swiss National Science Foundation. J.P. was supported by an ETH Zurich Seed Grant. R.S. was supported by the Bill & Melinda Gates Foundation. J.S. was supported by a Health Grand Challenges Grant from Princeton University. Author contributions: T.P.V.B., S.B., and R.L. designed the study. T.P.V.B. performed the analysis and wrote the first version of the manuscript. J.P., J.S., R.S., and C.Z. conducted literature reviews. J.P. and N.G.C. developed resistancebank.org. All authors contributed to the final version of the manuscript. Competing interests: R.L. is chair of the board for HealthCubed and GARDP. The authors declare no other competing interests. Data and materials availability: resistancebank.org is supported by ETH Zurich and hosted by shinyapps.io. Data are also available at https://dataverse.harvard.edu/dataverse/resistancebank. R code is available at Zenodo (37).
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ETH Zurich
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RE: Leapfrogging antimicrobial use in food production
Van Boeckel et al. are right to sound the alarm on antibiotic use and resistance within farmed animals and the looming public health emergency resulting from this practice. It is true that there is a rapidly-closing window of opportunity in emerging economies to avoid slipping into the systems of intensive animal farming that have spurred this irresponsible antibiotic usage in the developed world. However, the most effective opportunity to seize here is not simply to improve farm biosecurity but rather to do away with animal farming altogether as a means of producing meat. A technological revolution is already underway for novel production methods for producing plant-based meat products or cultivated meat (farming animal cells directly rather than whole animals). These approaches allow emerging economies to leapfrog over industrialized animal agriculture as a whole, alleviating not just the public health threat of antimicrobial resistance but also a whole host of externalized harms associated with intensive animal farming operations — including water and air pollution and severe animal welfare concerns. Governments in both the developed and developing world should be devoting substantially more resources toward these innovative approaches for entirely eradicating antibiotic use in food production rather than partially mitigating the harms associated with current practices.