How effective are strategies to control the dissemination of antibiotic resistance in the environment? A systematic review
2020
Goulas, Anais | Belhadi, Drifa | Descamps, Alexandre | Andremont, Antoine | Benoit, Pierre | Courtois, Sophie | Dagot, Christophe | Grall, Nathalie | Makowski, David | Nazaret, Sylvie | Nelieu, Sylvie | Patureau, Dominique | Petit, Fabienne | Roose-Amsaleg, Céline | Vittecoq, Marion | Livoreil, Barbara | Laouénan, Cédric | Infection, Anti-microbiens, Modélisation, Evolution (IAME (UMR_S_1137 / U1137)) ; Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris Cité (UPCité)-Université Sorbonne Paris Nord | Fondation pour la recherche sur la Biodiversité (FRB) | Département d'épidémiologie, biostatistique et recherche clinique ; Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-AP-HP - Hôpital Bichat - Claude Bernard [Paris] ; Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP) | Ecologie fonctionnelle et écotoxicologie des agroécosystèmes (ECOSYS) ; AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Centre International de Recherche Sur l'Eau et l'Environnement [Suez] (CIRSEE) ; SUEZ ENVIRONNEMENT (FRANCE) | Anti-infectieux : supports moléculaires des résistances et innovations thérapeutiques (RESINFIT) ; CHU Limoges-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Génomique, Environnement, Immunité, Santé, Thérapeutique (GEIST) ; Université de Limoges (UNILIM)-Université de Limoges (UNILIM) | Agronomie ; AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Centre International de Recherche sur l'Environnement et le Développement (CIRED) ; Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École des hautes études en sciences sociales (EHESS)-AgroParisTech-École nationale des ponts et chaussées (ENPC)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS) | Laboratoire d'Ecologie Microbienne - UMR 5557 (LEM) ; Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-Ecole Nationale Vétérinaire de Lyon (ENVL)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Laboratoire de Biotechnologie de l'Environnement [Narbonne] (LBE) ; Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Morphodynamique Continentale et Côtière (M2C) ; Université de Caen Normandie (UNICAEN) ; Normandie Université (NU)-Normandie Université (NU)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Rouen Normandie (UNIROUEN) ; Normandie Université (NU)-Centre National de la Recherche Scientifique (CNRS) | Milieux Environnementaux, Transferts et Interactions dans les hydrosystèmes et les Sols (METIS) ; École Pratique des Hautes Études (EPHE) ; Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Institut national des sciences de l'Univers (INSU - CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS) | Ecosystèmes, biodiversité, évolution [Rennes] (ECOBIO) ; Université de Rennes (UR)-Institut Ecologie et Environnement - CNRS Ecologie et Environnement (INEE-CNRS) ; Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) | Institut de recherche de la Tour du Valat | French Ministry of Ecological and Inclusive Transition (CGDD/SR, DGPR); Foundation for Research on Biodiversity (FRB) ; SUEZ company.
(IF 4.93; Q1)
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Show more [+] Less [-]English. Background: Antibiotic resistance is a major concern for public and environmental health. The role played by the environment in disseminating resistance is increasingly considered, as well as its capacity for mitigation. We reviewed the literature on strategies to control dissemination of antibiotic-resistant bacteria (ARB), antibiotic resistance genes (ARG) and mobile genetic elements (MGE) in the environment. Methods: This systematic review focused on three main strategies: (i) restriction of antibiotic use (S1), (ii) treatments of liquid/solid matrices (S2) and (iii) management of natural environment (S3). Articles were collected from seven scientific databases until July 2017 and from Web of Science until June 2018. Only studies reporting measurements of ARB, ARG or MGE in environmental samples were included. An evidence map was drawn from metadata extracted from all studies eligible for S1, S2 and S3. Subsets of studies were assessed for internal and external validity to perform narrative and quantitative syntheses. A meta-analysis was carried out to assess the effects of organic waste treatments (random-effect models). Review findings: Nine hundred and thirty-one articles representing 1316 individual studies (n) were eligible for S1 (n = 59), S2 (n = 781) and S3 (n = 476) strategies, respectively. Effects of interventions to control the dissemination of antibiotic resistance in the environment were primarily studied in strategy S2. A partial efficiency of wastewater treatment plants (WWTPs) to reduce antibiotic resistance in treated effluent was reported in 118 high validity studies. In spite of the heterogeneity in published results, the meta-analysis showed that composting and drying were efficient treatments to reduce the relative abundance of ARG and MGE in organic waste, by 84% [65%; 93%] and 98% [80%; 100%], respectively. The effect of anaerobic digestion was not statistically significant (51% reduction [− 2%; 77%]) when organic waste treatments were compared together in the same model. Studies in strategies S1 and S3 mainly assessed the effects of exposure to sources of contamination. For instance, 28 medium/high validity studies showed an increase of antibiotic resistance in aquatic environments at the WWTP discharge point. Some of these studies also showed a decrease of resistance as the distance from the WWTP increases, related to a natural resilience capacity of aquatic environments. Concerning wildlife, nine medium/high validity studies showed that animals exposed to anthropogenic activities carried more ARB. Conclusions and implications : Knowledge gaps were identified for the relationship between restriction of antibiotic use and variation of antibiotic resistance in the environment, as well as on possible interventions in situ in natural environment. Organic waste treatments with thermophilic phase (> 50 °C) should be implemented before the use/release of organic waste in the environment. More investigation should be conducted with the datasets available in this review to determine the treatment efficiency on ARG carried by specific bacterial communities.
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