Management Options for Reducing the Release of Antibiotics and Antibiotic Resistance Genes to the Environment

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Abstract

Background: There is growing concern worldwide about the role of polluted soil and water environments in the development and dissemination of antibiotic resistance.

Objective: Our aim in this study was to identify management options for reducing the spread of antibiotics and antibiotic-resistance determinants via environmental pathways, with the ultimate goal of extending the useful life span of antibiotics. We also examined incentives and disincentives for action.

Methods: We focused on management options with respect to limiting agricultural sources; treatment of domestic, hospital, and industrial wastewater; and aquaculture.

Discussion: We identified several options, such as nutrient management, runoff control, and infrastructure upgrades. Where appropriate, a cross-section of examples from various regions of the world is provided. The importance of monitoring and validating effectiveness of management strategies is also highlighted. Finally, we describe a case study in Sweden that illustrates the critical role of communication to engage stakeholders and promote action.

Conclusions: Environmental releases of antibiotics and antibiotic-resistant bacteria can in many cases be reduced at little or no cost. Some management options are synergistic with existing policies and goals. The anticipated benefit is an extended useful life span for current and future antibiotics. Although risk reductions are often difficult to quantify, the severity of accelerating worldwide morbidity and mortality rates associated with antibiotic resistance strongly indicate the need for action.

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Most cited references 105

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Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study

Karthikeyan K Kumarasamy, Mark Toleman, Timothy R. Walsh … (2010)

Summary Background Gram-negative Enterobacteriaceae with resistance to carbapenem conferred by New Delhi metallo-β-lactamase 1 (NDM-1) are potentially a major global health problem. We investigated the prevalence of NDM-1, in multidrug-resistant Enterobacteriaceae in India, Pakistan, and the UK. Methods Enterobacteriaceae isolates were studied from two major centres in India—Chennai (south India), Haryana (north India)—and those referred to the UK's national reference laboratory. Antibiotic susceptibilities were assessed, and the presence of the carbapenem resistance gene bla NDM-1 was established by PCR. Isolates were typed by pulsed-field gel electrophoresis of XbaI-restricted genomic DNA. Plasmids were analysed by S1 nuclease digestion and PCR typing. Case data for UK patients were reviewed for evidence of travel and recent admission to hospitals in India or Pakistan. Findings We identified 44 isolates with NDM-1 in Chennai, 26 in Haryana, 37 in the UK, and 73 in other sites in India and Pakistan. NDM-1 was mostly found among Escherichia coli (36) and Klebsiella pneumoniae (111), which were highly resistant to all antibiotics except to tigecycline and colistin. K pneumoniae isolates from Haryana were clonal but NDM-1 producers from the UK and Chennai were clonally diverse. Most isolates carried the NDM-1 gene on plasmids: those from UK and Chennai were readily transferable whereas those from Haryana were not conjugative. Many of the UK NDM-1 positive patients had travelled to India or Pakistan within the past year, or had links with these countries. Interpretation The potential of NDM-1 to be a worldwide public health problem is great, and co-ordinated international surveillance is needed. Funding European Union, Wellcome Trust, and Wyeth.

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A molecular view of microbial diversity and the biosphere.

N Pace (1997)

Over three decades of molecular-phylogenetic studies, researchers have compiled an increasingly robust map of evolutionary diversification showing that the main diversity of life is microbial, distributed among three primary relatedness groups or domains: Archaea, Bacteria, and Eucarya. The general properties of representatives of the three domains indicate that the earliest life was based on inorganic nutrition and that photosynthesis and use of organic compounds for carbon and energy metabolism came comparatively later. The application of molecular-phylogenetic methods to study natural microbial ecosystems without the traditional requirement for cultivation has resulted in the discovery of many unexpected evolutionary lineages; members of some of these lineages are only distantly related to known organisms but are sufficiently abundant that they are likely to have impact on the chemistry of the biosphere.

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Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study.

Timothy R. Walsh, Janis Weeks, David M. Livermore … (2011)

Not all patients infected with NDM-1-positive bacteria have a history of hospital admission in India, and extended-spectrum β-lactamases are known to be circulating in the Indian community. We therefore measured the prevalence of the NDM-1 gene in drinking water and seepage samples in New Delhi. Swabs absorbing about 100 μL of seepage water (ie, water pools in streets or rivulets) and 15 mL samples of public tap water were collected from sites within a 12 km radius of central New Delhi, with each site photographed and documented. Samples were transported to the UK and tested for the presence of the NDM-1 gene, bla(NDM-1), by PCR and DNA probing. As a control group, 100 μL sewage effluent samples were taken from the Cardiff Wastewater Treatment Works, Tremorfa, Wales. Bacteria from all samples were recovered and examined for bla(NDM-1) by PCR and sequencing. We identified NDM-1-positive isolates, undertook susceptibility testing, and, where appropriate, typed the isolates. We undertook Inc typing on bla(NDM-1)-positive plasmids. Transconjugants were created to assess plasmid transfer frequency and its relation to temperature. From Sept 26 to Oct 10, 2010, 171 seepage samples and 50 tap water samples from New Delhi and 70 sewage effluent samples from Cardiff Wastewater Treatment Works were collected. We detected bla(NDM-1) in two of 50 drinking-water samples and 51 of 171 seepage samples from New Delhi; the gene was not found in any sample from Cardiff. Bacteria with bla(NDM-1) were grown from 12 of 171 seepage samples and two of 50 water samples, and included 11 species in which NDM-1 has not previously been reported, including Shigella boydii and Vibrio cholerae. Carriage by enterobacteria, aeromonads, and V cholera was stable, generally transmissible, and associated with resistance patterns typical for NDM-1; carriage by non-fermenters was unstable in many cases and not associated with typical resistance. 20 strains of bacteria were found in the samples, 12 of which carried bla(NDM-1) on plasmids, which ranged in size from 140 to 400 kb. Isolates of Aeromonas caviae and V cholerae carried bla(NDM-1) on chromosomes. Conjugative transfer was more common at 30°C than at 25°C or 37°C. The presence of NDM-1 β-lactamase-producing bacteria in environmental samples in New Delhi has important implications for people living in the city who are reliant on public water and sanitation facilities. International surveillance of resistance, incorporating environmental sampling as well as examination of clinical isolates, needs to be established as a priority. European Union. Copyright © 2011 Elsevier Ltd. All rights reserved.

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Author and article information

Journal

Journal ID (nlm-ta): Environ Health Perspect

Journal ID (iso-abbrev): Environ. Health Perspect

Journal ID (publisher-id): EHP

Title: Environmental Health Perspectives

Publisher: National Institute of Environmental Health Sciences

ISSN (Print): 0091-6765

ISSN (Electronic): 1552-9924

Publication date (Electronic): 04 June 2013

Publication date (Print): August 2013

Volume: 121

Issue: 8

Pages: 878-885

Affiliations

[1 ]Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, Virginia, USA

[2 ]Institute for Biomedicine, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

[3 ]Unilever-Safety & Environmental Assurance Centre, Sharnbrook, United Kingdom

[4 ]Australian National University, Canberra, Australia

[5 ]Canberra Hospital, Canberra, Australia

[6 ]Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, Denmark

[7 ]School of Civil Engineering and Geosciences, Newcastle University, Newcastle upon Tyne, United Kingdom

[8 ]Office of Research and Development, U.S. Environmental Protection Agency, Cincinnati, Ohio, USA

[9 ]Center for Marine Environmental Studies, Ehime University, Matsuyama, Ehime, Japan

[10 ]MB Consult Limited, Southampton, United Kingdom

[11 ]University of Bradford, Bradford, United Kingdom

[12 ]AstraZeneca, Brixham Environmental Laboratory, Brixham, United Kingdom

[13 ]Agriculture and Agri-Food Canada, London, Ontario, Canada

[14 ]Department of Civil Engineering, University of Hong Kong, Hong Kong

[15 ]Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, China

Author notes

Address correspondence to D.G. Joakim Larsson, Department of Infectious Diseases, Institute for Biomedicine, The Sahlgrenska Academy, University of Gothenburg, Guldhedsgatan 10, SE-413 46, Göteborg, Sweden. Telephone: 46 31 786 3589. E-mail: joakim.larsson@ 123456fysiologi.gu.se

[*]

These authors contributed equally to this work.

Article

Publisher ID: ehp.1206446

DOI: 10.1289/ehp.1206446

PMC ID: 3734499

PubMed ID: 23735422

SO-VID: 87007e35-389d-468b-bc9d-f08cff3d8bb9

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, properly cited.

History

Date received : 19 December 2012

Date accepted : 30 May 2013

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Most cited references 105

Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study

A molecular view of microbial diversity and the biosphere.

Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study.

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