Skip to main content
Log in

The effect of conventional wastewater treatment on the levels of antimicrobial-resistant bacteria in effluent: a meta-analysis of current studies

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

Antimicrobial agents in the environment are a cause for concern. Antimicrobial drug residues and their metabolites reach the aquatic and terrestrial environment primarily through wastewater treatment plants (WWTP). In addition to the potential direct negative health and environmental effects, there is potential for the development of antimicrobial-resistant bacteria. Residue levels below the minimum inhibitory concentration for a bacterial species can be important in selection of resistance. There is uncertainty associated with resistance formation during WWTP processing. A meta-analysis study was carried out to analyse the effect of WWTP processing on the levels of antimicrobial-resistant bacteria within bacterial populations. An analysis of publications relating to multiple antimicrobial-resistant (MAR) bacteria (n = 61), single antimicrobial-resistant (SAR) E. coli (n = 81) and quinolone/fluoroquinolone-resistant (FR) bacteria (n = 19) was carried out. The odds-ratio (OR) of MAR (OR = 1.60, p < 0.01), SAR (OR = 1.33, p < 0.01) and FR (OR = 1.19, p < 0.01) bacteria was determined. The results infer that WWTP processing results in an increase in the proportion of resistant bacteria in effluent, even though the overall bacterial population may have reduced (i.e. a reduction in total bacterial numbers but an increase in the percentage of resistant bacteria). The results support the need for further research into the development of antimicrobial-resistant strains and possible selective pressures operating in WWTPs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bax, L. (2010). MIX 2.0. Professional software for meta-analysis in Excel. Version (2.0.0.7) (2.0 ed.), BiostatXL.

  • Bax, L., Yu, L.-M., Ikeda, N., Tsuruta, H., & Moons, K. (2006). Development and validation of MIX: Comprehensive free software for meta-analysis of causal research data. BMC Medical Research Methodology, 6(1), 50.

    Article  Google Scholar 

  • Bax, L., Yu, L. M., Ikeda, N., Tsuruta, H., & Moons, K. G. M. (2008). MIX: Comprehensive free software for meta-analysis of causal research data (1.7 ed.).

  • Bell, J. B., Elliott, G. E., & Smith, D. W. (1983). Influence of sewage treatment and urbanization on selection of multiple resistance in fecal coliform populations. Applied and Environment Microbiology, 46(1), 227–232.

    CAS  Google Scholar 

  • Chalmers, T. C., Levin, H., Sacks, H. S., Reitman, D., Berrier, J., & Nagalingam, R. (1987). Meta-analysis of clinical trials as a scientific discipline. I: Control of bias and comparison with large co-operative trials (Vol. 6). New York: Wiley Subscription Services, Inc., A Wiley Company.

  • Coffey, R., Bergin, D., & Cummins, E. (2010). Use of meta-analysis to assess the effect of conventional water treatment methods on the prevalence of cryptosporidium spp. in drinking water. Human and Ecological Risk Assessment, 16(6), 1360–1378.

    Article  CAS  Google Scholar 

  • Cummins, E. (2008). The role of quantitative risk assessment in the management of foodborne biological hazards. International Journal of Risk Assessment and Management, 8(3), 318–330.

    Article  Google Scholar 

  • Cummins, E., Kennedy, R., & Cormican, M. (2010). Quantitative risk assessment of Cryptosporidium in tap water in Ireland. Science of the Total Environment, 408(4), 740–753.

    Article  CAS  Google Scholar 

  • DeCoster, J. (2009). Meta-analysis notes. Retrieved October 15th 2010. http://www.stat-help.com/Meta%20analysis%202009-07-31.pdf.

  • DerSimonian, R., & Laird, N. (1986). Meta-analysis in clinical trials. Controlled Clinical Trials, 7(3), 177–188.

    Article  CAS  Google Scholar 

  • Easterbrook, P. J., & Berlin, J. A. (1991). Publication bias in clinical research. Lancet, 337(8746), 867.

    Article  CAS  Google Scholar 

  • Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315(7109), 629–634.

    Article  CAS  Google Scholar 

  • Ferreira da Silva, M., Vaz-Moreira, I., Gonzalez-Pajuelo, M., Nunes, O. C., & Manaia, C. M. (2007). Antimicrobial resistance patterns in Enterobacteriaceae isolated from an urban wastewater treatment plant. FEMS Microbiology Ecology, 60(1), 166–176.

    Article  CAS  Google Scholar 

  • Gallert, C., Fund, K., & Winter, J. (2005). Antibiotic resistance of bacteria in raw and biologically treated sewage and in groundwater below leaking sewers (Vol. 69, Applied Microbiology & Biotechnology): Springer Science & Business Media B.V.

  • Garcia, S., Wade, B., & Bauer, C. (2007). The effect of wastewater treatment on antibiotic resistance in Escherichia coli and enterococcus sp. [Feature]. Water Environment Research, 79(12), 2387–2395.

    Article  CAS  Google Scholar 

  • George, I., Crop, P., & Servais, P. (2002). Fecal coliform removal in wastewater treatment plants studied by plate counts and enzymatic methods. Water Research, 36(10), 2607–2617.

    Article  CAS  Google Scholar 

  • Greenhouse, J. B., & Iyengar, S. (1994). Sensitivity analysis and diagnostics. In H. Cooper & L. Hedges (Eds.), Handbook of research synthesis (pp. 383–398). New York, NY: Russel Sage Foundation.

    Google Scholar 

  • Grimwood, K., Collignon, P. J., Currie, B. J., Ferson, M. J., Gilbert, G. L., Hogg, G. G., et al. (1997). Antibiotic management of pneumococcal infections in an era of increased resistance. Journal of Paediatrics and Child Health, 33(4), 287–295.

    Article  CAS  Google Scholar 

  • Hassani, L., Imziln, B., & Gauthier, M. J. (1992). Antibiotic-resistant Escherichia coli from wastewater before and after treatment in stabilization ponds in the arid region of Marrakech, Morocco. Letters in Applied Microbiology, 15(5), 228–231.

    Article  Google Scholar 

  • Hirsch, R., Ternes, T., Haberer, K., & Kratz, K.-L. (1999). Occurrence of antibiotics in the aquatic environment. The Science of the Total Environment, 225(1–2), 109–118.

    Article  CAS  Google Scholar 

  • HPSC. (2008). Consumption of antibiotics in public acute hospitals in Ireland 2008 data.

  • Ibrahim, E. H., Sherman, G., Ward, S., Fraser, V. J., & Kollef, M. H. (2000). The influence of inadequate antimicrobial treatment of bloodstream infections on patient outcomes in the ICU setting (Vol. 118, CHEST). American College of Chest Physicians.

  • Ioannidis, J., & Trikalinos, T. A. (2007). The appropriateness of asymmetry tests for publication bias in meta-analyses: A large survey. Canadian Medical Association Journal, 176(8), 1091.

    Article  Google Scholar 

  • Jakobsen, L., Sandvang, D., Hansen, L. H., Bagger-Skjøt, L., Westh, H., Jørgensen, C., et al. (2008). Characterisation, dissemination and persistence of gentamicin resistant Escherichia coli from a Danish university hospital to the waste water environment. Environment International, 34(1), 108–115.

    Article  CAS  Google Scholar 

  • Kumarasamy, K. K., Toleman, M. A., Walsh, T. R., Bagaria, J., Butt, F., Balakrishnan, R., et al. (2011). Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. The Lancet Infectious Diseases, 10(9), 597–602.

    Article  Google Scholar 

  • Kümmerer, K. (2008). Pharmaceuticals in the environment: Sources, fate, effects and risks (3rd ed.). Berlin, Germany: Springer.

    Google Scholar 

  • L’Abbe, K. A., Detsky, A. S., & O’Rourke, K. (1987). Meta-analysis in clinical research. Annals of Internal Medicine, 107(2), 224–233.

    Google Scholar 

  • Lefkowitz, J. R., & Duran, M. (2009). Changes in antibiotic resistance patterns of escherichia coli during domestic wastewater treatment. Water Environment Research, 81, 878–885.

    Article  CAS  Google Scholar 

  • Lipsey, M. W., & Wilson, D. B. (2001). Practical meta-analysis (Vol. 49, Applied social research methods series). California, USA: SAGE.

  • Manaia, C., Novo, A., Coelho, B., & Nunes, O. (2010). Ciprofloxacin resistance in domestic wastewater treatment plants. Water, Air, and Soil Pollution, 208, 335–343.

    Article  CAS  Google Scholar 

  • Murray, G. E., Tobin, R. S., Junkins, B., & Kushner, D. J. (1984). Effect of chlorination on antibiotic resistance profiles of sewage-related bacteria. Applied and Environment Microbiology, 48(1), 73–77.

    CAS  Google Scholar 

  • Nicolas-Chanoine, M.-H., Blanco, J., Leflon-Guibout, V., Demarty, R., Alonso, M. P., Canica, M. M., et al. (2007). Intercontinental emergence of Escherichia coli clone O25:H4-ST131 producing CTX-M-15. Journal of Antimicrobial Chemotherapy, dkm464. doi:10.1093/jac/dkm464.

  • O’Brien, N., & Cummins, E. (2010). Nano-scale pollutants: Fate in Irish surface and drinking water regulatory systems. Human and Ecological Risk Assessment: An International Journal, 16(4), 847–872.

    Article  Google Scholar 

  • Ochman, H., Lawrence, J. G., & Groisman, E. A. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature, 405(6784), 299–304.

    Article  CAS  Google Scholar 

  • Payment, P., Plante, R., & Cejka, P. (2001). Removal of indicator bacteria, human enteric viruses, Giardia cysts, and Cryptosporidium oocysts at a large wastewater primary treatment facility. Canadian Journal of Microbiology, 47, 188–193.

    CAS  Google Scholar 

  • Reinthaler, F. F., Posch, J., Feierl, G., Wüst, G., Haas, D., Ruckenbauer, G., et al. (2003). Antibiotic resistance of E. coli in sewage and sludge. Water Research, 37(8), 1685–1690.

    Article  CAS  Google Scholar 

  • Rolston, K. V. I. (2009). Bacterial infection in neutropenic cancer patients: An overview. Iranian Journal of Clinical Infectious Diseases, 4(2), 115–122.

    Google Scholar 

  • Salgado, C. D., Dash, S., Cantey, J. R., & Marculescu, C. E. (2007). Higher risk of failure of methicillin-resistant staphylococcus aureus prosthetic joint infections. Clinical Orthopaedics and Related Research, 461, 48–53.

    Google Scholar 

  • Samuelsen, Ø., Thilesen, C. M., Heggelund, L., Vada, A. N., Kümmel, A., & Sundsfjord, A. (2011). Identification of NDM-1-producing enterobacteriaceae in Norway. Journal of Antimicrobial Chemotherapy, 66(3), 670.

    Article  CAS  Google Scholar 

  • Sanders, C. C., Sanders, W. E. J., Goering, R. V., & Werner, V. (1984). Selection of multiple antibiotic resistance by quinolones, beta-lactams, and aminoglycosides with special reference to cross-resistance between unrelated drug classes. Antimicrobial Agents and Chemotherapy, 26(6), 797–801. doi:10.1128/aac.

    Article  CAS  Google Scholar 

  • Silva, J., Castillo, G., Callejas, L., Lopez, H., & Olmos, J. (2006). Frequency of transferable multiple antibiotic resistance amongst coliform bacteria isolated from a treated sewage effluent in Antofagasta, Chile. Electronic Journal of Biotechnology, 9(5), 533–540.

    Article  Google Scholar 

  • Varma, M., Field, R., Stinson, M., Rukovets, B., Wymer, L., & Haugland, R. (2009). Quantitative real-time PCR analysis of total and propidium monoazide-resistant fecal indicator bacteria in wastewater. Water Research, 43(19), 4790–4801.

    Article  CAS  Google Scholar 

  • Watkinson, A. J., Micalizzi, G. B., Graham, G. M., Bates, J. B., & Costanzo, S. D. (2007). Antibiotic resistant Escherichia coli in wastewaters, surface waters and oysters from an urban riverine system. Applied and Environmental Microbiology, AEM.00763-00707. doi:10.1128/aem.00763-07.

  • Whitehead, A. (2002). Meta-analysis of controlled clinical trials. Sussex, England: Wiley.

    Book  Google Scholar 

  • Wiener, J., Quinn, J. P., Bradford, P. A., Goering, R. V., Nathan, C., Bush, K., et al. (1999). Multiple antibiotic-resistant klebsiella and escherichia coli in nursing homes. JAMA, 281(6), 517–523. doi:10.1001/jama.281.6.517.

    Article  CAS  Google Scholar 

  • Zhang, Y., Marrs, C. F., Simon, C., & Xi, C. (2009). Wastewater treatment contributes to selective increase of antibiotic resistance among Acinetobacter spp. Science of the Total Environment, 407(12), 3702–3706.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge the Irish EPA for the funding of this project, under the STRIVE programme (2007-2013).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Enda Cummins.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harris, S., Cormican, M. & Cummins, E. The effect of conventional wastewater treatment on the levels of antimicrobial-resistant bacteria in effluent: a meta-analysis of current studies. Environ Geochem Health 34, 749–762 (2012). https://doi.org/10.1007/s10653-012-9493-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-012-9493-8

Keywords

Navigation