Elsevier

Science of The Total Environment

Volume 447, 1 March 2013, Pages 345-360
Science of The Total Environment

Review
Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: A review

https://doi.org/10.1016/j.scitotenv.2013.01.032Get rights and content

Abstract

Urban wastewater treatment plants (UWTPs) are among the main sources of antibiotics' release into the environment. The occurrence of antibiotics may promote the selection of antibiotic resistance genes (ARGs) and antibiotic resistant bacteria (ARB), which shade health risks to humans and animals. In this paper the fate of ARB and ARGs in UWTPs, focusing on different processes/technologies (i.e., biological processes, advanced treatment technologies and disinfection), was critically reviewed. The mechanisms by which biological processes influence the development/selection of ARB and ARGs transfer are still poorly understood. Advanced treatment technologies and disinfection process are regarded as a major tool to control the spread of ARB into the environment. In spite of intense efforts made over the last years to bring solutions to control antibiotic resistance spread in the environment, there are still important gaps to fill in. In particular, it is important to: (i) improve risk assessment studies in order to allow accurate estimates about the maximal abundance of ARB in UWTPs effluents that would not pose risks for human and environmental health; (ii) understand the factors and mechanisms that drive antibiotic resistance maintenance and selection in wastewater habitats. The final objective is to implement wastewater treatment technologies capable of assuring the production of UWTPs effluents with an acceptable level of ARB.

Graphical abstract

Highlights

► UWTPs may positively affect ARB spread and selection as well as ARG transfer. ► Resistance integrons may be used to characterize ARG transfer. ► High trough technologies are a useful complementation of PCR technologies. ► Biological process effect on ARB and ARG transfer should be further investigated. ► Advanced treatments/disinfection effect should be further investigated too.

Introduction

The intensive use of antibiotics for human, veterinary and agricultural purposes, results in their continuous release into the environment (Batt et al., 2006, Brown et al., 2006, Díaz-Cruz et al., 2003, Kümmerer, 2009). The main concern for the release of antibiotics into the environment is related to the development of antibiotic resistance genes (ARGs) and bacteria (ARB), which reduce the therapeutic potential against human and animal pathogens (Kemper, 2008, Zhang et al., 2009b). The increasing interest of the scientific community and international institutions/organization for this problem is respectively testified by the number of publications reviewed in this paper and internationally/scientifically relevant initiatives, such as research projects (e.g., PHARMAS) and networking (e.g., COST Action DARE).

Effluents from urban wastewater treatment plants (UWTPs) are suspected to be among the main anthropogenic sources for antibiotics (no maximum contaminant levels have been set by EU and other international institutions/organizations), ARGs and ARB spread into the environment (Ferreira da Silva et al., 2006, Figueira et al., 2011a, Kümmerer, 2009, Lupo et al., 2012). The biological treatment process creates an environment potentially suitable for resistance development and spread because bacteria are continuously mixed with antibiotics at sub-inhibitory concentrations (Auerbach et al., 2007, Davies et al., 2006, Ferreira da Silva et al., 2006). The knowledge regarding the effects of sub-inhibitory concentrations of anti-microbials and their effects on environmental bacteria, is scarce and contradictory especially with respect to resistance (Kümmerer, 2009).

ARBs are mostly studied in bacteria belonging to the common indicators of faecal contamination, namely coliforms and enterococci (Araújo et al., 2010, Boczek et al., 2007, Figueira et al., 2011a, Martins da Costa et al., 2006, Reinthaler et al., 2003, Sabate et al., 2008). The search for agents associated with human “difficult-to-treat infections” such as methicillin resistant Staphylococcus aureus, vancomycin resistant Entereococcus spp., and Gram-negative bacteria (enterobacteria, pseudomonads, acinetobacter) resistant to fluoroquinolones, carbapenems and producers of extended spectrum beta-lactamase, has also been addressed in such studies. Although at low percentages, when compared to what is observed in the clinical settings, antibiotic resistance profiles are often detected in wastewaters and recreational waters; a fact that may represent a relevant public health issue (Araújo et al., 2010, Soge et al., 2009). However, the current knowledge on the prevalence and types of antibiotic resistance in the environment is barely sufficient. In contrast to what has been done over the last years in the standardization and organization of antibiotic resistance data of clinical origin (ECDC, European Centre for Disease Prevention, Control, 2012, EUCAST, European Committee on Antimicrobial Susceptibility Testing, 2011), information regarding resistance of environmental bacteria is still very fragmented.

UWTPs typically include different processes (e.g., mechanical, biological, physical, chemical and physical–chemical) which may affect the fate of antibiotics, ARB and ARGs in different ways and consequently the development and spread of resistance into the environment. Accordingly, the aim of the present paper is to critically review the fate of ARB and ARGs in UWTPs. In particular, the effect of different processes/technologies, namely biological processes, advanced treatment technologies and disinfection, is addressed. Moreover, methods for the characterization/evaluation of ARB, ARGs and genes transfer are presented and discussed in a comprehensive way to facilitate the understanding of the effect of wastewater treatment processes/technologies on ARB and ARGs.

Section snippets

Tools to assess antibiotic resistance in UWTPs

The relationship existing between antibiotic consumption and the emergence and development of resistances is now well documented (Davies, 2007). If the acquisition of mutations widely contributes to bacterial adaptation, the exchange and reshuffling of genetic material between bacteria involving mobile genetic elements are the main contributors explaining the rapid dissemination of antibiotic resistances (Courvalin, 2008). Identifying hotspots of possible ARG dissemination starts by determining

Antibiotic resistance in UWTPs

Over the last years a renewed interest on the antibiotic resistance phenotypes in UWTPs became apparent in the scientific literature (Baquero et al., 2008, Kümmerer, 2009, Manaia et al., 2012). Human and animal commensal bacteria and other of environmental origin have been the major focus of these studies on antibiotic resistance in wastewaters. Given their close contact with humans and easiness to isolate and identify, the indicators of faecal contamination, coliforms and enterococci, are

Concluding remarks

The main conclusions that can be withdrawn based on the scientific literature available on the fate of ARB and ARGs in UWTPs, can be summarized as follows:

  • In spite of the lack of information as well as systematic and conclusive studies on the effect of biological process on antibiotic resistance, some studies showed that conventional UWTPs may positively affect ARB spread and selection as well as ARG transfer. Moreover, general trends of antibiotic resistance in relevant human-related

Acknowledgements

The authors wish to thank the EU for the support by Cost Action “TD0803: Detecting evolutionary hotspots of antibiotic resistances in Europe (DARE)”. Luigi Rizzo wishes to thank the University of Salerno for funding the project “Effect of solar photolysis on antibiotic degradation, antibiotic resistant bacteria inactivation as well as on their capacity to develop antibiotic resistance in surface water”, Ex 60%, anno 2011. Christophe Merlin and Christophe Dagot wish to thank the ANR national

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