Abstract

Antimicrobial resistance (AMR) is a major global public health concern, shared by a large number of human and animal health actors. Within the framework of a One Health approach, actions should be implemented in the environmental realm, as well as the human and animal realms. The Government of France commissioned a report to provide policy and decision makers with an evidential basis for recommending or taking future actions to mitigate AMR in the environment. We first examined the mechanisms that underlie the emergence and persistence of antimicrobial resistance in the environment. This report drew up an inventory of the contamination of aquatic and terrestrial environments by AMR and antibiotics, anticipating that the findings will be representative of some other high-income countries. Effluents of wastewater treatment plants were identified as the major source of contamination on French territory, with spreading of organic waste products as a more diffuse and incidental contamination of aquatic environments. A limitation of this review is the heterogeneity of available data in space and time, as well as the lack of data for certain sources. Comparing the French Measured Environmental Concentrations (MECs) with predicted no effect concentrations (PNECs), fluoroquinolones and trimethoprim were identified as representing high and medium risk of favoring the selection of resistant bacteria in treated wastewater and in the most contaminated rivers. All other antibiotic molecules analyzed (erythromycin, clarithromycin, azithromycin, tetracycline) were at low risk of resistance selection in those environments. However, the heterogeneity of the data available impairs their full exploitation. Consequently, we listed indicators to survey AMR and antibiotics in the environment and recommended the harmonization of sampling strategies and endpoints for analyses. Finally, the objectives and methods used for the present work could comprise a useful example for how national authorities of countries sharing common socio-geographic characteristics with France could seek to better understand and define the environmental dimension of AMR in their particular settings.

Highlights

  • The development of resistance of bacterial pathogens to antibiotics has greatly complicated the treatment of life-threatening bacterial in­ fections (Cassini et al, 2019; Furuya and Lowy, 2006; O’Neill, 2014)

  • If antimicrobial resistance (AMR, meaning resistance of bac­ terial commensals or pathogens to antimicrobial drugs) development proceed at the current rate, it is predicted that “if no action is taken”, drug resistant infections will account for 10 million global deaths each year by 2050, outpacing those caused by cancers (O’Neill, 2014)

  • The French Government commissioned a detailed report on the state of Antimicrobial resistance (AMR) in the aquatic and terrestrial envi­ ronments of this country based on the One Health approach

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Summary

Context

The development of resistance of bacterial pathogens to antibiotics has greatly complicated the treatment of life-threatening bacterial in­ fections (Cassini et al, 2019; Furuya and Lowy, 2006; O’Neill, 2014). If antimicrobial resistance (AMR, meaning resistance of bac­ terial commensals or pathogens to antimicrobial drugs) development proceed at the current rate, it is predicted that “if no action is taken”, drug resistant infections will account for 10 million global deaths each year by 2050, outpacing those caused by cancers (O’Neill, 2014) Within this context, national and international authorities have developed and are deploying action plans to mitigate the development of AMR (Comite interministeriel pour la sante, 2016; European Commission, 2017; WHO et al, 2020; World Health Organization, 2015). On the other hand, taking into account the role of the environment in the develop­ ment and transmission of AMR is recent, and actions in the environ­ mental sector are currently the least implemented in the framework of public policies (European Commission, 2019; Munkholm et al, 2021; Singer et al, 2016) Within this context, the French Government commissioned a detailed report on the state of AMR in the aquatic and terrestrial envi­ ronments of this country based on the One Health approach. The French situation is applicable to countries that share similar attributes; the more variance from these characteristics, the less applicable the analysis will be

Geographical and health characteristics of France
Objectives
Working group
Data and method of expertise
Investigated compartments
At the scale of the bacterium
At the scale of the bacterial community
Transfer of ARGs to pathogenic bacterial species in the environment
Mechanisms that govern bioavailability and bioaccessibility of antibiotic
Environmental contamination by antibiotics in France
Aquatic environments and sources of contamination
Terrestrial environments and sources of contamination
Contamination by ARB and ARGs
ARB and ARGs in wastewater effluents
ARB and ARGs in surface and ground water
ARB and ARGs in organic waste products
ARB and ARGs in soil
Wildlife as a reservoir for ARB and ARGs
Perspectives and recommendations
Limitations
Placing the One Health concept on a global scale
Broaden the panel of matrices and sources tested
Anticipate climate change impacts on AMR in the environment
Findings
Plan and act using a ’one health’ approach
Full Text
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