Abstract
It is generally accepted that intervention strategies to curb antibiotic resistance cannot solely focus on human and veterinary medicine but must also consider environmental settings. While the environment clearly has a role in transmission of resistant bacteria, its role in the emergence of novel antibiotic resistance genes (ARGs) is less clear. It has been suggested that the environment constitutes an enormous recruitment ground for ARGs to pathogens, but its extent is practically unknown. We have constructed a model framework for resistance emergence and used available quantitative data on relevant processes to identify limiting steps in the appearance of ARGs in human pathogens. We found that in a majority of possible scenarios, the environment would only play a minor role in the emergence of novel ARGs. However, the uncertainty is enormous, highlighting an urgent need for more quantitative data. Specifically, more data is most needed on the fitness costs of ARG carriage, the degree of dispersal of resistant bacteria from the environment to humans, and the rates of mobilization and horizontal transfer of ARGs. This type of data is instrumental to determine which processes should be targeted for interventions to curb development and transmission of ARGs in the environment.
Highlights
Antibiotic resistance is a globally growing health threat, which is projected to take more lives than all forms of cancer combined by 2050 if it cannot be controlled.[1]
While surveillance programs and careful reduction of the use of antibiotics in clinical and agricultural settings started years ago, we are still only starting to understand the role of the environment in the development and dissemination of antibiotic resistance.[3−5] Monitoring data on the abundance and diversity of antibiotic resistance genes (ARGs) has provided a conceptual understanding of the dispersal routes for ARGs between and within humans, farmed animals and the external environment.[6−8] We have a reasonably clear picture of what processes result in recruitment of ARGs from environmental bacteria to human pathogens.[9]
It is likely that ARGs that are present in human pathogens already pre-existed in bacteria in some setting at the start of the antibiotic era and only needed to be, in some way, transferred to human pathogens.[17−19] This scenario is our main model in this study
Summary
Antibiotic resistance is a globally growing health threat, which is projected to take more lives than all forms of cancer combined by 2050 if it cannot be controlled.[1]. It has been proposed that the environment could have three main roles in resistance development.[9] First, it enables the transfer of ARGs between environmental, human, and animal associated bacteria. It constitutes a reservoir or intermediate habitat for resistant bacteria and ARGs. Second, it constitutes a reservoir or intermediate habitat for resistant bacteria and ARGs It can play a crucial role in the evolution of novel resistance factors, as it provides an arena for selection of resistance combined with an enormous source of genetic diversity from which bacteria can recruit ARGs.[8,9] In this paper, we have chosen to use the definitions of Bengtsson-Palme et al.[9] and defined the “emergence” of an ARG as the event where it first appears in a context in which it provides operational resistance.[11] a gene is considered to be “mobilized” when it appears on a mobile genetic element (MGE), such as a plasmid, transposon, or integron. Emerged ARGs from the environment can subsequently be disseminated into the human and farmed animals’ compartments, where they have the potential to cause severe health threats
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