A conceptual framework for the environmental surveillance of antibiotics and antibiotic resistance

Environmental surveillance of antibiotics and antibiotic resistance could contribute toward the protection of human, animal and ecosystem health. However, justification for the choice of markers and sampling sites that informs about different risk scenarios is often lacking. Here, we define five fundamentally different objectives for surveillance of antibiotics and antibiotic resistance in the environment. The first objective is (1) to address the risk of transmission of already antibiotic-resistant bacteria to humans via environmental routes. The second is (2) to address the risk for accelerating the evolution of antibiotic resistance in pathogens through pollution with selective agents and bacteria of human or animal origin. The third objective is (3) to address the risks antibiotics pose for aquatic and terrestrial ecosystem health, including the effects on ecosystem functions and services. The two final objectives overlap with those of traditional clinical surveillance, namely, to identify (4) the population-level resistance prevalence and (5) population-level antibiotic use. The latter two environmental surveillance objectives have particular potential in countries where traditional clinical surveillance data and antibiotic consumption data are scarce or absent. For each objective, the levels of evidence provided by different phenotypic and genotypic microbial surveillance markers, as well as antibiotic residues, are discussed and evaluated on a conceptual level. Furthermore, sites where monitoring would be particularly informative are identified. The proposed framework could be one of the starting points for guiding environmental monitoring and surveillance of antibiotics and antibiotic resistance on various spatiotemporal scales, as well as for harmonizing such activities with existing human and animal surveillance systems.