Selective pressure of antibiotic pollution on bacteria of importance to public health
Abstract
Background: Many bacteria of clinical importance survive and may grow in different environments. Antibiotic pollution may exert on them a selective pressure leading to an increase in the prevalence of resistance. Objectives: In this study we sought to determine whether environmental concentrations of antibiotics and concentrations representing action limits used in environmental risk assessment may exert a selective pressure on clinically relevant bacteria in the environment. Methods: We used bacterial inhibition as an assessment end point to link antibiotic selective pressures to the prevalence of resistance in bacterial populations. Species sensitivity distributions were derived for three antibiotics by fitting log-logistic models to end points calculated from minimum inhibitory concentration (MIC) distributions based on worldwide data collated by the European Committee on Antimicrobial Susceptibility Testing (EUCAST). To place bacteria represented in these distributions in a broader context, we performed a brief phylogenetic analysis. The potentially affected fraction of bacterial genera at measured environmental concentrations of antibiotics and environmental risk assessment action limits was used as a proxy for antibiotic selective pressure. Measured environmental concentrations and environmental risk assessment action limits were also directly compared to wild-type cut-off values. Results: The potentially affected fraction of bacterial genera estimated based on antibiotic concentrations measured in water environments is ≤ 7%. We estimated that measured environmental concentrations in river sediments, swine feces lagoons, liquid manure, and farmed soil inhibit wild-type populations in up to 60%, 92%, 100%, and 30% of bacterial genera, respectively. At concentrations used as action limits in environmental risk assessment, erythromycin and ciprofloxacin were estimated to inhibit wild-type populations in up to 25% and 76% of bacterial genera. Conclusions: Measured environmental concentrations of antibiotics, as well as concentrations representing environmental risk assessment action limits, are high enough to exert a selective pressure on clinically relevant bacteria that may lead to an increase in the prevalence of resistance.
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Antibiotic resistance is ubiquitous in the environment but is exacerbated in places with diverse bacterial communities and pronounced anthropogenic pollution.
“Antibiotic resistance is considered ubiquitous in the environment but is exacerbated in places with diverse bacterial communities and pro nounced anthropogenic pollution (Finley et al., 2013; Tello et al., 2012).”
From Review of emerging contaminants in green stormwater infrastructure: antibiotic resistance genes, microplastics, tire wear particles, PFAS, and temperature (2024) · cites this paper as Tello et al., 2012
The Conclusions identify antibiotic-polluted river sediments, liquid manure, and farmed soil as likely hot spots for the development of resistance. The Discussion says pollution has the potential to increase resistance in clinically relevant bacteria. Our copy does not establish that resistance is ubiquitous in the environment or that bacterial community diversity itself exacerbates it. (LLM, conf=0.84)
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Research works printed but not linked: 41
- Agersø Y Wulff G Vaclavik E Halling-Sørensen B Jensen LB 2006 Effect of tetracycline residues in pig manure slurry on tetracycline-resistant bacteria and resistance gene tet(M) in soil microcosms. Environ Int 32 876 882 16808974
- Bonfiglio G Livermore DM 1991 Effect of media composition on the susceptibility of Xanthomonas mahophilia to β-lactam antibiotics. J Antimicrob Chemother 28 837 842 1816181
- Butler T Frenck RW Johnson RB Khakhria R 2001 In vitro effects of azithromycin on Salmonella typhi: early inhibition by concentrations less than the MIC and reduction of MIC by alkaline pH and small inocula. J Antimicrob Chemother 47 455 458 11266420
- Chander Y Kumar K Goyal SM Gupta SC 2005 Antibacterial activity of soil-bound antibiotics. J Environ Qual 34 1952 1957 16221813
- Chopra I Roberts M 2001 Tetracycline antibiotics: mode of action, applications, molecular biology and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65 232 260 11381101 PMC99026
- Ciric L Mullany P Roberts AP 2011 Antibiotic and antiseptic resistance genes are linked on a novel mobile genetic element: Tn6087. J Antimicrob Chemother; doi: 10.1093/jac/dkr311 [Online 3 August 2011] PMC3172042 21816764 · DOI
- Clewell DB Flannagan SE Jaworski DD 1995 Unconstrained bacterial promiscuity: the Tn916-Tn1545 family of conjugative transposons. Trends Microbiol 3 229 236 7648031
- Córdova-Kreylos AL Scow KM 2007 Effects of ciprofloxacin on salt marsh sediment microbial communities. ISME J 1 585 595 18043666
- de Knecht J Boucard T Brooks BW Crane M Eirkson C Gerould S 2009 Environmental risk assessment and management of veterinary medicines In Veterinary Medicines in the Environment (Crane M, Boxall ABA, Barrett K, eds). Boca Raton, FL:CRC Press, 21–55
- EMEA (European Medicines Agency) 2006 Guideline on the Environmental Risk Assessment of Medicinal Products for Human Use. EMEA/CHMP/SWP/4447/00 corr 1. London:EMEA. Available: http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2009/10/WC500003978.pdf [accessed 15 June 2012]
- Golet EM Strehler A Alder AC Giger W 2002 Determination of fluoroquinolone antibacterial agents in sewage sludge and sludge-treated soil using accelerated solvent extraction followed by solid-phase extraction. Anal Chem 74 5455 5462 12433073
- Grist EPM Leung KMY Wheeler JR Crane M 2002 Better bootstrap estimation of hazardous concentration thresholds for aquatic assemblages. Environ Toxicol Chem 21 1515 1524 12109754
- Hamscher G 2006 Veterinary pharmaceuticals In Organic Pollutants in the Water Cycle (Reemtsma T, Jekel M, eds). Berlin:Wiley-VCH, 99–120
- Hoffman LR D’Argenio DA MacCoss MJ Zhang Z Jones RA Miller SI 2005 Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436 1171 1175 16121184
- Idowu OR Peggins JO Cullison R Bredow JV 2010 Comparative pharmacokinetics of enrofloxacin and ciprofloxacin in lactating dairy cows and beef steers following intravenous administration of enrofloxacin. Res Vet Sci 89 230 235 20129633
- Kahlmeter G Brown DFJ Goldstein FW MacGowan AP Mouton JW Österlund A 2003 European harmonization of MIC breakpoints for antimicrobial susceptibility testing of bacteria. J Antimicrob Chemother 52 145 148 12837738
- Kimura M 1980 A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16 111 120 7463489
- Knapp CW Dolfing J Ehlert PAI Graham DW 2010 Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol 44 580 587 20025282
- Knapp CW Engemann CA Hanson ML Keen PL Hall KJ Graham DW 2008 Indirect evidence of transposon-mediated selection of antibiotic resistance genes in aquatic systems at low-level oxytetracycline exposures. Environ Sci Technol 42 5348 5353 18754392
- Kolpin DW Furlong ET Meyer MT Thurman EM Zaugg SD Barber LB 2002 Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams 1999–2000: a national reconnaissance. Environ SciTechnol 36 1202 1211 11944670
- Kristiansson E Fick J Janzon A Grabic R Rutgersson C Weijdegård B 2011 Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS ONE 6 2; doi: 10.1371/journal.pone.0017038 [Online 16 February 2011] PMC3040208 21359229 · DOI
- Kümmerer K 2009a The presence of pharmaceuticals in the environment due to human use—present knowledge and future challenges. J Environ Manage 90 2354 2366 19261375
- Kümmerer K 2009b Antibiotics in the aquatic environment—a review—part II. Chemosphere 75 435 441 19178931
- Ludwig W Strunk O Westram R Richter L Meier H Buchner A 2004 ARB: a software environment for sequence data. Nucleic Acids Res 32 1363 1371 14985472 PMC390282
- Luo Y Xu L Rysz M Wang Y Zhang H Alvarez PJJ 2011 Occurrence and transport of tetracycline sulfonamide quinolone and macrolide antibiotics in the Haihe River Basin, China. Environ Sci Technol 45 1827 1833 21309601
- MacGowan AP Wise R 2001 Establishing MIC breakpoints and the interpretation of in vitro susceptibility tests. J Antimicrob Chemother 48 suppl 1: 17 28 11420334
- Madigan MT Martinko JM Dunlap PV Clark DP 2009 Brock Biology of Microorganisms San Francisco:Pearson
- Martinez JL 2008 Antibiotics and antibiotic resistance genes in natural environments. Science 321 365 367 18635792
- Martinez JL 2009 Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157 2893 2902 19560847
- Michel JP Yeh PJ Chait R Moellering RC Kishony R 2008 Drug interactions modulate the potential for evolution of resistance. Proc Natl Acad Sci USA 105 14918 14923 18815368 PMC2567468
- Moriarty E Nourozi F Robson B Wood D Gilpin B 2008 Evidence for growth on enterococci in municipal oxidation ponds obtained using antibiotic resistance analysis. Appl Environ Microbiol 74 7204 7210 18836001 PMC2592925
- Paradis E Strimmer K 2004 APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20 289 290 14734327
- Pei R Cha J Carlson KH Pruden A 2007 Response of antibiotic resistance genes (ARG) to biological treatment in dairy lagoon water. Environ SciTechnol 41 5108 5113 17711231
- Saitou N Nei M 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406 425 3447015
- Sarmah AK Meyer MT Boxall ABA 2006 A global perspective on the use, sales, exposure pathways occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65 725 759 16677683
- Schmitt H Stoob K Hamscher G Smit E Seinen W 2006 Tetracyclines and tetracycline resistance in agricultural soils: microcosm and field studies. Microb Ecol 51 267 276 16598633
- Schön T Juréen P Giske CG Chryssanthou E Sturegård E Werngren J 2009 Evaluation of wild-type MIC distributions as a tool for determination of clinical breakpoints for Mycobacterium tuberculosis. J Antimicrob Chemother 64 786 793 19633001
- Topp E Welsh M Tien YC Dang A Lazarovits G Conn K 2003 Strain-dependent variability in growth and survival of Escherichia coli in agricultural soil. FEMS Microbiol Lett 44 44: 303 308 19719611
- Turnidge J Paterson DL 2007 Setting and revising antibacterial susceptibility breakpoints. Clin Microbiol Rev 20 391 408 17630331 PMC1932754
- Wright GD 2010 Antibiotic resistance in the environment: a link to the clinic? Curr Opin Microbiol 13 589 594 20850375
- Yarza P Richter M Peplies J Euzeby J Amann R Schleifer KH 2008 The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31 241 250 18692976
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Bodus, B., O'Malley, K., Dieter, G., Gunawardana, C., & McDonald, W. (2024) · Science of The Total Environment · doi:10.1016/j.scitotenv.2023.167195 · Cited by 76 · see citing works
- Authors
- Tello, A., Austin, B., & Telfer, T. C.
- Affiliations
- Institute of Aquaculture, University of Stirling, Stirling, Scotland, United Kingdom
- Venue
- Environmental Health Perspectives
- Publisher
- American Chemical Society (ACS)
- Published
- 2012-05-08
- Volume
- 120
- Issue
- 8
- Pages
- 1100-1106
- ISSN
- 0091-6765
- 1552-9924
- PMC
- PMC3440082
- Cited by
- 332
- References
- 0
- Language
- en
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