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Bacteria from Animals As a Pool of Antimicrobial Resistance Genes

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Bacteria from Animals As a Pool of Antimicrobial Resistance Genes antibiotics Review Bacteria from Animals as a Pool of Antimicrobial Resistance Genes Maria Angeles Argudín 1,*, Ariane Deplano 1, Alaeddine Meghraoui 1, Magali Dodémont 1, Amelie Heinrichs 1, Olivier Denis 1,2, Claire Nonhoff 1 and Sandrine Roisin 1 1 National Reference Centre—Staphylococcus aureus, Department of Microbiology, Hôpital Erasme, Université Libre de Bruxelles, Route de Lennik 808, 1070 Brussels, Belgium; [email protected] (A.D.); [email protected](A.M.); [email protected] (M.D.); [email protected] (A.H.); [email protected] (O.D.); [email protected](C.N.); [email protected] (S.R.) 2 Ecole de Santé Publique, Université Libre de Bruxelles, Avenue Franklin Roosevelt 50, 1050 Bruxelles, Belgium * Correspondence: [email protected]; Tel.: +32-25-556-971 Academic Editor: Mary Barton Received: 27 March 2017; Accepted: 1 June 2017; Published: 6 June 2017 Abstract: Antimicrobial agents are used in both veterinary and human medicine. The intensive use of antimicrobials in animals may promote the fixation of antimicrobial resistance genes in bacteria, which may be zoonotic or capable to transfer these genes to human-adapted pathogens or to human gut microbiota via direct contact, food or the environment. This review summarizes the current knowledge of the use of antimicrobial agents in animal health and explores the role of bacteria from animals as a pool of antimicrobial resistance genes for human bacteria. This review focused in relevant examples within the ESC(K)APE (Enterococcus faecium, Staphylococcus aureus, Clostridium difficile (Klebsiella pneumoniae), Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacteriaceae) group of bacterial pathogens that are the leading cause of nosocomial infections throughout the world. Keywords: mec; cfr; mcr 1. Introduction The discovery of antimicrobial agents in the mid-twentieth century revolutionized the management and therapy of bacterial infections. Infections that would normally have been fatal became curable. Ever since then, the antimicrobial agents have saved the lives of millions of people. However, these gains are now seriously jeopardized by the rapid emergence and spread of antimicrobial-resistant bacteria [1]. Antimicrobial resistance (AMR) is a major health problem rapidly spreading across the world. The Review on Antimicrobial Resistance report [2] estimates that at least 700,000 annual deaths are due to infections by drug-resistant strains of common bacterial infections, human immunodeficiency virus (HIV), tuberculosis and malaria. Numbers suggested that up to 50,000 lives are lost each year due to antibiotic-resistant infections in Europe and the US alone [2]. The inappropriate use of antibiotics in food animals, as well as in the medical practice has potentiated the risk of untreatable infections. Due to the free movement of people and goods between countries, and the intensive international transport of livestock, the problem of AMR is becoming by nature a global problem. Moreover, the AMR emergence is accompanied with a decline in the discovery of new antimicrobial agents. It has been estimated that most of the antibiotics used presently for common human and animal infections will be useless within five to ten years, turning back the clock to the pre-antibiotic era [1]. Antimicrobial agents are principally used for therapy and prevention of human and animal diseases, but they are still used in some countries for growth-promotion in food animal productions [3]. Antibiotics 2017, 6, 12; doi:10.3390/antibiotics6020012 www.mdpi.com/journal/antibiotics AntibioticsAntibiotics2017 2017, 6,, 12 6, 12 2 of2 38 of 38 Antimicrobial agents are principally used for therapy and prevention of human and animal Theirdiseases, indiscriminate but they are use still has used contributed in some countries to the for emergence growth‐promotion of bacterial in food resistance, animal productions in hospitals, community[3]. Their andindiscriminate livestock settings. use has AMRcontributed may spread to the fromemergence animals of bacterial to humans resistance, and vice in versa; hospitals, directly bycommunity the spread and of the livestock resistant settings. bacteria AMR or may indirectly spread from by the animals spread to ofhumans resistance and vice genes versa; from directly animal bacteriaby the to spread human of bacteria.the resistant In thisbacteria manuscript, or indirectly we overviewby the spread the currentof resistance knowledge genes from about animal the use of antimicrobialbacteria to human agents bacteria. of critical In this importance manuscript, in we veterinary overview the medicine, current andknowledge investigate about the the potentialuse of of bacteriaantimicrobial from agents animals of ascritical an AMR-gene importance reservoir. in veterinary We have medicine, also underlined and investigate some the resistance potential genes of thatbacteria were firstly from animals described as an in AMR bacteria‐gene from reservoir. animals We have and also later underlined were found some in resistance human bacteria. genes that This were firstly described in bacteria from animals and later were found in human bacteria. This review review focused in relevant examples within the ESKAPE (Enterococcus faecium, Staphylococcus aureus, focused in relevant examples within the ESKAPE (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter spp.) or ESCAPE Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter spp.) or (E. faecium, S. aureus, Clostridium difficile, A. baumannii, P. aeruginosa, and Enterobacteriaceae) bacterial ESCAPE (E. faecium, S. aureus, Clostridium difficile, A. baumannii, P. aeruginosa, and Enterobacteriaceae) pathogensbacterial that pathogens are the that leading are the cause leading of nosocomial cause of nosocomial infections infections throughout throughout the world the [ 4world,5]. [4,5]. 2. Use of Antimicrobials in Animal Health 2. Use of Antimicrobials in Animal Health AntimicrobialAntimicrobial agents agents play play a a keykey rolerole inin thethe treatment of of bacterial bacterial infections infections in inhuman human and and veterinaryveterinary medicine. medicine. In In fact, fact, AMR AMR has has been been consideredconsidered the the quintessential quintessential One One Health Health issue issue [6]. [ 6This]. This OneOne Health Health approach approach recognizes recognizes that that thethe humanhuman health is is connected connected to to the the animal animal health health and and the the environmentenvironment [7 ].[7]. TheThe use use of of antimicrobials antimicrobials in in veterinary veterinary medicinemedicine creates creates a a selective selective pressure pressure for for the the emergence emergence of antimicrobialof antimicrobial resistant resistant bacteria, bacteria, including including animalanimal pathogens, human human pathogens pathogens that that have have animal animal reservoirsreservoirs and and commensal commensal bacteria bacteria from from animals animals [[8]8] The bacteria bacteria selected selected by by this this pressure pressure can can spread spread to humansto humans either either by by direct direct contact contact with with animalsanimals or food products, products, or or indirectly indirectly via via environmental environmental pathwayspathways and/or and/or non-food non‐food producing producing animalsanimals [8] [8] (Figure (Figure 1).1). Wildlife Companion animals (rodents, birds, etc.) Direct contact Humans Food animals Food Community Health system Environment Vegetables, seed Water Soil crops and fruits FigureFigure 1. Interactions1. Interactions between between groups. groups. Antimicrobial-resistantAntimicrobial‐resistant bacteria bacteria can can spread spread to tohumans humans either either byby the the food food supply, supply, direct direct contact contact with with foodfood or companion animals animals or, or, more more indirectly, indirectly, through through environmentalenvironmental pathways, pathways, including including waterways,waterways, soils and and vegetables vegetables contaminated contaminated with with human human or or animals waste, and vectors such as rodents, insects, and birds. Based on da Costa et al. [8] and animals waste, and vectors such as rodents, insects, and birds. Based on da Costa et al. [8] and McEwen et al. [9] with modifications. McEwen et al. [9] with modifications. The antimicrobial use in animals selects for AMR in commensal and zoonotic bacteria [9]. Soil treatedThe antimicrobial with manure represents use in animals a “hot spot” selects of bacteria for AMR carrying in commensal AMR‐genes and [10]. zoonotic However, bacteria soil itself [9]. Soilis treated also a natural with manure reservoir represents for antimicrobial a “hot spot”‐resistant of bacteria bacteria carrying [10]. The AMR-genes fecal wastes [10 ].from However, animals soil itselfcontaminate is also a natural groundwater, reservoir streams for antimicrobial-resistant and other waterways, bacteria contributing [10]. The to fecal the spread wastes of from bacteria animals contaminatecarrying AMR groundwater,‐genes [9]. streams Human and wastes other waterways,from homes, contributing hospitals and to the offices spread also of bacteriacontribute carrying to AMR-genescontaminate [9]. Humanrivers and wastes waterways from homes, with hospitals antimicrobial and offices‐resistant
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