Global antimicrobial-resistance drivers: an ecological country-level study at the human-animal interface

Background Antimicrobial resistance (AMR) is a pressing, holistic, and multisectoral challenge facing contemporary global health. In this study we assessed the associations between socioeconomic, anthropogenic, and environmental indicators and country-level rates of AMR in humans and food-producing animals. Methods In this modelling study, we obtained data on Carbapenem-resistant Acinetobacter baumanii and Pseudomonas aeruginosa, third generation cephalosporins-resistant Escherichia coli and Klebsiella pneumoniae, oxacillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus faecium AMR in humans and food-producing animals from publicly available sources, including WHO, World Bank, and Center for Disease Dynamics Economics and Policy. AMR in food-producing animals presented a combined prevalence of AMR exposure in cattle, pigs, and chickens. We used multivariable beta regression models to determine the adjusted association between human and food-producing animal AMR rates and an array of ecological country-level indicators. Human AMR rates were classified according to the WHO priority pathogens list and antibiotic-bacterium pairs. Findings Significant associations were identified between animal antimicrobial consumption and AMR in foodproducing animals (OR 1 center dot 05 [95% CI 1 center dot 01-1 center dot 10]; p=0 center dot 013), and between human antimicrobial consumption and AMR specifically in WHO critical priority (1 center dot 06 [1 center dot 00-1 center dot 12]; p=0 center dot 035) and high priority (1 center dot 22 [1 center dot 09-1 center dot 37]; p<0 center dot 0001) pathogens. Bidirectional associations were also found: animal antibiotic consumption was positively linked with resistance in critical priority human pathogens (1 center dot 07 [1 center dot 01-1 center dot 13]; p=0 center dot 020) and human antibiotic consumption was positively linked with animal AMR (1 center dot 05 [1 center dot 01-1 center dot 09]; p=0 center dot 010). Carbapenem-resistant Acinetobacter baumanii, third generation cephalosporins-resistant Escherichia coli, and oxacillin-resistant Staphylococcus aureus all had significant associations with animal antibiotic consumption. Analyses also suggested significant roles of socioeconomics, including governance on AMR rates in humans and animals. Interpretation Reduced rates of antibiotic consumption alone will not be sufficient to combat the rising worldwide prevalence of AMR. Control methods should focus on poverty reduction and aim to prevent AMR transmission across different One Health domains while accounting for domain-specific risk factors. The levelling up of livestock surveillance systems to better match those reporting on human AMR, and, strengthening all surveillance efforts, particularly in low-income and middle-income countries, are pressing priorities.

Automated summary

This study assessed the associations between socioeconomic, anthropogenic, and environmental indicators and country-level rates of antimicrobial resistance (AMR) in humans and food-producing animals. The results showed that there were significant associations between animal antimicrobial consumption and AMR in food-producing animals, as well as between human antimicrobial consumption and AMR in WHO priority pathogens. Bidirectional associations were also found between animal antibiotic consumption and resistance in critical priority human pathogens, and between human antibiotic consumption and animal AMR. This study suggests that reducing antibiotic consumption alone is not enough to combat the rising prevalence of AMR, and control methods should focus on poverty reduction and preventing AMR transmission across different domains.