Abstract
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.
Generated Summary
This research article uses point prevalence surveys from low- and middle-income countries (LMICs) to map trends in antimicrobial resistance (AMR) in animals. The study’s approach involved analyzing 901 surveys reporting AMR rates in animals for common indicator pathogens, including Escherichia coli, Campylobacter spp., nontyphoidal Salmonella spp., and Staphylococcus aureus. Geospatial models were employed to generate global maps of AMR in LMICs, providing a baseline for monitoring AMR levels in animals and guiding targeted interventions. The researchers aimed to address the challenges of comparing surveys with different protocols and identifying indicator organisms. They also sought to create composite metrics to summarize global trends and improve the interpolation of epidemiological observations from data-rich regions to data-poor regions. The focus was on understanding the global scale-up of demand for animal protein, its impact on antimicrobial usage, and the consequences of AMR in animals, considering that the majority of antimicrobials are used in food-producing animals. The main goal was to provide policy-makers with insights to tackle the issue of AMR in animals.
Key Findings & Statistics
- Meat production has increased significantly since 2000, with 68%, 64%, and 40% growth in Asia, Africa, and South America, respectively, while plateauing in high-income countries.
- 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, with cattle showing a plateau between 0.12 and 0.23.
- The number of published surveys on resistance in LMICs increased from three in 2000 to 121 in 2018, peaking at 156 per year in 2017.
- The number of surveys per country was not correlated with gross domestic product (GDP) per capita.
- The study estimated that across LMICs, 9% of cattle, 18% of pigs, and 21% of chickens were raised in AMR hotspots in 2013.
- In chickens, the percentage of birds raised in hotspots of resistance exceeded the global average in China (38%), Egypt (38%), and Turkey (72%).
- In LMICs, the average yearly increase in P50 was 1.5%/year for chickens and 1.3%/year for pigs.
- Hotspots of resistance (P50 > 0.4) were predicted in various regions, including northeastern India, northeastern China, and southern Brazil.
- The highest resistance rates were observed for tetracyclines, sulfonamides, and penicillins, the most commonly used classes of antimicrobials in animal production.
- Resistance to ciprofloxacin and erythromycin was high (20 to 60%), and moderate for third- and fourth-generation cephalosporins (10 to 40%).
- Colistin resistance was high (18 to 40%) in Asia.
- In Campylobacter spp., resistance rates were high for tetracycline (60%) and quinolones (60%).
- Across all antimicrobials, resistance rates for S. aureus were higher in Asia.
- In 2013, the percentage of chickens raised in hotspots of AMR in each country exceeded the global average in China (38%), Egypt (38%), and Turkey (72%).
Other Important Findings
- Hotspots of AMR were identified 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 starting to emerge include Kenya, Morocco, Uruguay, southern Brazil, central India, and southern China.
- The difference between P10 and P50 was high (>0.5) in Kenya, Morocco, Uruguay, southern and eastern Brazil, central India, Iran, Chile, and southern China, indicating emerging AMR hotspots.
- Established hotspots of AMR (P10 – P50 < 0.1) included northeastern China, West Bengal, and Turkey.
- The travel time to cities of 50,000 people was the leading factor associated with the geographic distribution of P50.
- The study found that in LMICs, E. coli and Campylobacter had resistance levels comparable with European levels but considerably higher than in the United States, where quinolones were banned in poultry in 2005.
- The authors suggest that regional restrictions on the use of specific compounds are associated with lower AMR rates.
Limitations Noted in the Document
- Insufficient geographic coverage may lead to inaccurate spatial predictions, and local variations in AMR might not reflect “ground truth.”
- The study did not account for temporal variation in AMR over the period 2000-2018.
- In slaughterhouse surveys, molecular typing was not performed longitudinally, which could have enabled assessment of cross-contamination.
- It is uncertain whether the study could draw conclusions about the intensity and directionality of transfer of AMR between animals and humans.
- The accuracy of the P50 maps reflects the density of surveys for a region.
- Geospatial models had limited accuracies.
- The association between P50 and temperature needs further investigation.
Conclusion
The study emphasizes the global challenge of antimicrobial resistance in animals, especially in LMICs, and underscores the urgent need for action. The authors highlight that the reliance on antimicrobials in intensive animal production systems is a threat to both animal health and the livelihoods of farmers, as well as human health. They recommend immediate actions in regions with the highest AMR levels to preserve the efficacy of essential antimicrobials, particularly by restricting their use in animal production. This would involve supporting a transition to sustainable animal farming practices. The geographic distribution of AMR hotspots reveals that the greatest burden is currently in Asia, where targeted interventions, such as legislative action and subsidies to improve farm hygiene, are crucial. In Africa, the study suggests a need for caution in applying overly aggressive measures that might undermine livestock-based economic development. High-income countries are encouraged to support the transition in LMICs through a global fund that improves farm-level biosafety and biosecurity. The study highlights the need for intensified surveillance in poorly surveyed regions, particularly in the Americas, to fully understand and address the spread of AMR effectively. The authors conclude by stressing the need for immediate action to preserve the efficacy of antimicrobials essential for human medicine and the importance of supporting sustainable animal production in LMICs through a global fund.
IFFS Team Summary
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