Vancomycin resistant enterococci: From the hospital effluent to the urban wastewater treatment plant

Science of the Total Environment

Volumn 450-451, Issue , 2013, Pages 155-161

  Varela, Ana Rita ^a   Ferro, Giovanna ^a,b   Vredenburg, Jana ^a   Yanik, Melike ^a   Vieira, Lucas ^a   Rizzo, Luigi ^b   Lameiras, Catarina ^c   Manaia, Célia M ^a  

^a UNIVERSIDADE CATÓLICA PORTUGUESA   (Portugal)

^b UNIVERSITY OF SALERNO   (Italy)

^c PORTUGUESE ONCOLOGY INSTITUTE   (Portugal)

Author keywords

Enterococci; Hospital; Urban wastewater treatment plant; Vancomycin

Indexed keywords

CIPROFLOXACIN; CLINICAL ISOLATES; CLINICAL PRACTICES; ENTEROCOCCI; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; FINAL EFFLUENTS; HOSPITAL EFFLUENT; HUMAN ACTIVITIES; RESISTANT BACTERIA; URBAN WASTEWATER; URBAN WASTEWATER TREATMENT PLANTS; VANCOMYCIN; VANCOMYCIN-RESISTANT ENTEROCOCCI;

ANTIBIOTICS; BACILLI; EFFLUENTS; SEWAGE; SEWAGE PUMPING PLANTS; TOXICITY; WATER TREATMENT PLANTS;

HOSPITALS;

AMOXICILLIN; CIPROFLOXACIN; COTRIMOXAZOLE; ERYTHROMYCIN; GENTAMICIN; TETRACYCLINE;

ANTIBIOTIC RESISTANCE; BACTERIUM; DISCHARGE; EFFLUENT; HUMAN ACTIVITY; POLLUTANT SOURCE; URBAN POLLUTION; WASTE TREATMENT; WASTEWATER;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM ISOLATE; BIOCHEMICAL OXYGEN DEMAND; CHEMICAL OXYGEN DEMAND; CIPROFLOXACIN RESISTANT ENTEROCOCCUS; CONTROLLED STUDY; EFFLUENT; ENTEROCOCCUS; ENTEROCOCCUS AVIUM; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS HIRAE; HOSPITAL WASTE; NONHUMAN; POLLUTION TRANSPORT; PRIORITY JOURNAL; URBAN AREA; VANCOMYCIN RESISTANT ENTEROCOCCUS; WASTE WATER TREATMENT PLANT;

ENTEROCOCCUS; ENVIRONMENTAL MONITORING; HOSPITAL BED CAPACITY, 500 AND OVER; HOSPITALS; PORTUGAL; VANCOMYCIN RESISTANCE; WASTE WATER; WATER MICROBIOLOGY; WATER PURIFICATION;

EID: 84874775428     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2013.02.015     Document Type: Article

References (44)

1. Aerestrup F.M., Agerso Y.P., Gerner-Smidt P., Madsen M., Jensen L.B. Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers, and pigs in Denmark. Diagn Microbiol Infect Dis 2000, 37:127-137.
2. Anon Water quality-detection and enumeration of intestinal enterococci-part 2: membrane filtration method (ISO 7899-2) 2000, International Organization for Standardization, Geneva.
3. Araújo C., Torres C., Silva N., Carneiro C., Gonçalves A., Radhouani H., et al. Vancomycin-resistant enterococci from Portuguese wastewater treatment plants. J Basic Microbiol 2010, 50:605-609.
4. Ashbolt N., Grabow W.O.K., Snozzi M. Indicators of microbial water quality. Water quality: guidelines, standards and health: assessment of risk and risk management for water-related infectious disease 2001, 289-316. IWA Publishing, London. L. Fewtrell, J. Bartram (Eds.).
5. Baker-Austin C., Wright M.S., Stepanauskas R., McArthur J.V. Co-selection of antibiotic and metal resistance. Trends Microbiol 2006, 14:176-182.
6. Baquero F., Martínez J.-L., Cantón R. Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 2008, 19:260-265.
7. Bonten M.J.M., Willems R., Weinstein R.A. Vancomycin-resistant enterococci: why are they here, and where do they come from?. Lancet Infect Dis 2001, 1:314-325.
8. Braoudaki M., Hilton A.C. Adaptive resistance to biocides in Salmonella enterica and Escherichia coli O157 and cross-resistance to antimicrobial agents. J Clin Microbiol 2004, 42:73-78.
9. Chun J., Lee J.H., Jung Y., Kim M., Kim S., Kim B.K., et al. EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 2007, 57:2259-2261.
10. CLSI Performance Standards for Antimicrobial Susceptibility Testing; Twenty-First Informational Supplement. CLSI document M100-S21 2011, Clinical and Laboratory Standards Institute, Wayne, PA.
11. Devriese L.A., Collins M.D., Wirth R. The genus Enterococcus. The prokaryotes 1992, 1466-1481. Springer-Verlag, New York, N.Y. 2nd ed. A. Balows, H.G. Truper, M. Dworkin, W. Harder, K.-H. Schleifer (Eds.).
12. Donskey C.J., Helfand M.S., Pultz N.J., Rice L.B. Effect of parenteral fluoroquinolone administration on persistence of vancomycin-resistant Enterococcus faecium in the mouse gastrointestinal tract. Antimicrob Agents Chemother 2004, 48:326-328.
13. Dutka-Malen S., Evers S., Courvalin P. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J Clin Microbiol 1995, 33:24-27.
14. ECDC - European Centre for Disease Prevention and Control (ECDC) Available from:, [Accessed August 2012]. http://ecdc.europa.eu/en/healthtopics/antimicrobial_resistance/Pages/index.aspx.
15. EU- Bathing Water Directive Directive 2006/7/EC of the European Parliament and of the Council of 15 February 2006 concerning the management of bathing water quality and repealing Directive76/160/EEC 2006.
16. EUCAST (European Committee on Antimicrobial Susceptibility Testing) MIC and Zone Diameter Distributions of Wild Type Microorganisms Available from:, [Accessed November 2012]. http://www.srga.org/eucastwt/wt_eucast.htm.
17. Ferreira Da Silva M., Tiago I., Verissimo A., Boaventura R.A.R., Nunes O.C., Manaia C.M. Antibiotic resistance of enterococci and related bacteria in an urban wastewater treatment plant. FEMS Microbiol Ecol 2006, 55:322-329.
18. Gerhard P.T., Murray R., Costilo W.R., Nester E., Wood W., Krieg N., et al. Manual of methods for general bacteriology 1981, American Society of Microbiology, Washington, DC.
19. Gonçalves A., Igrejas G., Radhouani H., López M., Guerra A., Petrucci-Fonseca F., et al. Detection of vancomycin-resistant enterococci from faecal samples of Iberian wolf and Iberian lynx, including Enterococcus faecium strains of CC17 and the new singleton ST573. Sci Total Environ 2011, 410-411:266-268.
20. Graham D.W., Olivares-Rieumont S., Knapp C.W., Lima L., Werner D., Bowen E. Antibiotic resistance gene abundances associated with waste discharges to the Almendares River near Havana Cuba. Environ Sci Technol 2011, 45:418-424.
21. Hasman H., Kempf I., Chidaine B., Cariolet R., Ersbøll A.K., Houe H., et al. Copper resistance in Enterococcus faecium, mediated by the tcrB gene, is selected by supplementation of pig feed with copper sulfate. Appl Environ Microbiol 2006, 72:5784-5789.
22. Hernandez A., Mellado R.P., Martinez J.L. Metal accumulation and vanadium-induced multidrug resistance by environmental isolates of Escherichia hermannii and Enterobacter cloacae. Appl Environ Microbiol 1998, 64:4317-4320.
23. Jensen L.B., Ahrens P., Dons L., Jones R.N., Hammerum A.M., Aarestrup F.M. Molecular analysis of Tn1546 in Enterococcus faecium isolated from animals and humans. J Clin Microbiol 1998, 36:437-442.
24. Klein G. Taxonomy, ecology and antibiotic resistance of enterococci from food and the gastro-intestinal tract. Int J Food Microbiol 2003, 88:123-131.
25. Kummerer K., Henninger A. Promoting resistance by the emission of antibiotics from hospitals and households into effluent. Clin Microbiol Infect 2003, 9:1203-1214.
26. Leavis H.L., Willems R.J.L., Top J., Bonten M.J.M. High-level ciprofloxacin resistance from point mutations in gyrA and parC confined to global hospital-adapted clonal lineage CC17 of Enterococcus faecium. J Clin Microbiol 2006, 44:1059-1064.
27. Lewis K. Persister cells. Annu Rev Microbiol 2010, 64:357-372.
28. Luczkiewicz A., Jankowska K., Fudala-Ksiazek S., Olanczuk-Neyman K. Antimicrobial resistance of fecal indicators in municipal wastewater treatment plant. Water Res 2010, 44:5089-5097.
29. Manaia C.M., Vaz-Moreira I., Nunes O.C. Antibiotic resistance in waste water and surface water and human health implications. Emerging organic contaminants and human health 2012, 173-212. Springer-Verlag, Berlin. D. Barceló (Ed.).
30. Martinez J.L. Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 2009, 157:2893-2902.
31. Martins da Costa P., Vaz-Pires P., Bernardo F. Antimicrobial resistance in Enterococcus spp. isolated in inflow, effluent and sludge from municipal sewage water treatment plants. Water Res 2006, 40:1735-1740.
32. Michael I., Rizzo L., McArdell C.S., Manaia C.M., Merlin C., Schwartz T., Dagot C., Fatta-Kassinos D. Urban wastewater treatment plants as hotspots for the release of antibiotics in the environment: a review. Water Res 2013, 47:957-995.
33. Nilsson O., Greko C., Bengtsson B. Environmental contamination by vancomycin resistant enterococci (VRE) in Swedish broiler production. Acta Vet Scand 2009, 51:49. 10.1186/1751-0147-51-49.
34. Novais C., Coque T.M., Ferreira H., Sousa J.C., Peixe L. Environmental contamination with vancomycin-resistant enterococci from hospital sewage in Portugal. Appl Environ Microbiol 2005, 71:3364-3368.
35. Novo A., Manaia C.M. Factors influencing antibiotic resistance burden in municipal waste water treatment plants. Appl Microbiol Biotechnol 2010, 87:1157-1166.
36. Novo A., André S., Viana P., Nunes O.C., Manaia C.M. Antibiotic resistance, antimicrobial residues and bacterial community composition in urban wastewater. Water Res 2013, 47:1875-1887.
37. Oberlé K., Capdeville M.J., Berthe T., Budzinski H., Petit F. Evidence for a complex relationship between antibiotics and antibiotic-resistant Escherichia coli: from medical center patients to a receiving environment. Environ Sci Technol 2012, 46:1859-1868.
38. Rizzo L., Manaia C.M., Merlin C., Schwartz T., Dagot C., Ploy M.C. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a Review. Sci Total Environ 2013, 447:345-360.
39. Sahlström L., Rehbinder V., Albihn A., Aspan A., Bengtsson B. Vancomycin resistant enterococci (VRE) in Swedish sewage sludge. Acta Vet Scand 2009, 51:24.
40. Siegel J.D., Rhinehart E., Jackson M., Chiarello L. The Healthcare Infection Control Practices Advisory Committee. Management of multidrug-resistant organisms in healthcare settings 2006, Centers for Disease Control and Prevention, Atlanta.
41. van der Steen L.F., Bonten M.J.M., van Kregten E., Charssema-Poot J.J.C., Willems R., Gaillard C.A. An outbreak of vancomycin- resistant Enterococcus faecium in a nephrology ward. Ned Tijdschr Geneeskd 2000, 144:2568-2571.
42. Werner G., Fleige C., Ewert B., Laverde-Gomez J.A., Klare I., Witte W. High-level ciprofloxacin resistance among hospital-adapted Enterococcus faecium (CC17). Int J Antimicrob Agents 2010, 35:119-125.
43. Willems R.J.L., Top J., van den Braak N., van Belkum A., Mevius D.J., Hendriks G., et al. Molecular diversity and evolutionary relationships of Tn1546-like elements in enterococci from humans and animals. Antimicrob Agents Chemother 1999, 43:483-491.
44. Woodford N., Abediyi A.M.M., Palepou M.F.I., Cookson B.D. Diversity of VanA glycopeptide resistance elements in enterococci from human and nonhuman sources. Antimicrob Agents Chemother 1998, 42:502-508.