«One Health» approach: transfer of antimicrobial resistance from animals to humans

Abstract

Antimicrobials are valuable therapeutics whose efficacy is seriously compromised by the emergence and spread of antimicrobial resistance. The current science provides overwhelming evidence that antibiotic use is a powerful selector of resistance that can appear not only at the point of origin but also nearly everywhere else. The latter phenomenon occurs because of the enormous ramifications of horizontal gene transfer. A mounting body of evidence shows that antimicrobial use in animals, including the nontherapeutic use of antimicrobials, leads to the propagation and shedding of substantial amounts of antimicrobial-resistant bacteria — both as pathogens, which can directly and indirectly infect humans, and as commensals, which may carry transferable resistance determinants across species borders and reach humans through multiple routes of transfer. These pathways include not only food but also water and sludge and manure applications to food crop soils. Continued nontherapeutic use of antimicrobials in food animals will increase the pool of resistance genes, as well as their density, as bacteria migrate into the environment at large. The lack of species barriers for gene transmission argues that the focus of research efforts should be directed toward the genetic infrastructure and that it is now imperative to take an ecological approach toward addressing the impacts of NTA use on human disease. The study of animal-to-human transmission of antibiotic resistance therefore requires a greater understanding of the genetic interaction and spread that occur in the larger arena of commensal and environmental bacteria. The provision of antibiotics to food animals encompasses a wide variety of nontherapeutic purposes that include growth promotion. The concern over resistance emergence and spread to people by nontherapeutic use of antimicrobials has led to conflicted practices and opinions. Considerable evidence supported the removal of nontherapeutic antimicrobials in Europe and North America, based on the «precautionary principle». Still, concrete scientific evidence of the favorable versus unfavorable consequences of nontherapeutic antimicrobials is not clear to all stakeholders. Substantial data show elevated antibiotic resistance in bacteria associated with animals fed nontherapeutic antimicrobials and their food products. This resistance spreads to other animals and humans-directly by contact and indirectly via the food chain, water, air, and manured and sludge-fertilized soils. Modern genetic techniques are making advances in deciphering the ecological impact of nontherapeutic antimicrobials, but modeling efforts are thwarted by deficits in key knowledge of microbial and antibiotic loads at each stage of the transmission chain. Still, the substantial and expanding volume of evidence reporting animal-to-human spread of resistant bacteria, including that arising from use of nontherapeutic antimicrobials, supports eliminating antibiotics use in order to reduce the growing environmental load of resistance genes.