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Multidrug-resistant Enterobacteriaceae from indoor air of an urban wastewater treatment plant

  • Juliana V. Teixeira
  • Pedro Cecílio
  • Daniela Gonçalves
  • Vítor J. P. Vilar
  • Eugénia Pinto
  • Helena N. FerreiraEmail author
Article

Abstract

Wastewater treatment plants (WWTPs) have been recognized as sources of bioaerosols that may act as vehicles for dissemination of pathogens and multidrug-resistant (MDR) bacteria. The occurrence of MDR Enterobacteriaceae in indoor air of an urban WWTP was investigated. A possible airborne contamination with extended-spectrum beta-lactamase (ESBL) and carbapenemase-producing Enterobacteriaceae was also explored. Fourteen of 39 Enterobacteriaceae isolates were MDR. These isolates were found at all sampling sites, mainly at the secondary sedimentation settings. The highest levels of resistance were detected in three different species: Enterobacter cloacae, Escherichia coli, and Citrobacter freundii. Furthermore, one of the airborne E. coli isolates was phenotypically characterized as an ESBL producer. Additionally, five isolates showed non-susceptibility to at least one carbapenem tested. The presence of genes encoding relevant beta-lactamase types in these ESBL-producing and carbapenem-resistant Enterobacteriaceae isolates was investigated by PCR. Results showed amplification for bla CTX-M and bla OXA. These findings are relevant both in terms of occupational/public health and of environmental dissemination of MDR bacteria.

Keywords

Airborne Enterobacteriaceae Multidrug-resistant ESBL Carbapenemase Wastewater treatment plant 

Notes

Acknowledgments

Financial support for this work was mainly provided by FCT (Fundação para a Ciência e a Tecnologia) under the projects PTDC/EQU-EQU/100554/2008 and CEQUIMED-PEst-OE/SAU/UI4040/2014. J.V. Teixeira would like to acknowledge her fellowship (SFRH/BD/78477/2011) supported by FCT

References

  1. Chagas, T. P., Seki, L. M., Cury, J. C., Oliveira, J. A., Davila, A. M., Silva, D. M., et al. (2011). Multiresistance, beta-lactamase-encoding genes and bacterial diversity in hospital wastewater in Rio de Janeiro, Brazil. Journal of Applied Microbiology, 111, 572–581.CrossRefGoogle Scholar
  2. Chapin, A., Rule, A., Gibson, K., Buckley, T., & Schwab, K. (2005). Airborne multidrug-resistant bacteria isolated from a concentrated swine feeding operation. Environmental Health Perspectives, 113, 137–142.Google Scholar
  3. CLSI, (2011). Performance standards for antimicrobial susceptibility testing; Twenty-first informational supplement M100-S21. Clinical and Laboratory Standards Institute (CLSI). 31.Google Scholar
  4. Coque, T. M., Baquero, F., Canton, R., (2008). Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Euro Surveillance 13.Google Scholar
  5. Dallenne, C., Da Costa, A., Decre, D., Favier, C., & Arlet, G. (2010). Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. Journal of Antimicrobial Chemotherapy, 65, 490–495.CrossRefGoogle Scholar
  6. ECDC. (2011). Risk assessment on the spread of carbapenemase-producing Enterobacteriaceae (CPE) through patient transfer between healthcare facilities, with special emphasis on cross-border transfer. Stockholm: ECDC Technical Report. European Centre for Disease Prevention and Control.Google Scholar
  7. ECDC/EMEA. (2009). The bacterial challenge: time to react (ECDC/EMEA Joint Technical Report). Stockholm: European Centre for Disease Prevention and Control.Google Scholar
  8. Figueira, V., Serra, E. A., Vaz-Moreira, I., Brandao, T. R., & Manaia, C. M. (2012). Comparison of ubiquitous antibiotic-resistant Enterobacteriaceae populations isolated from wastewaters, surface waters and drinking waters. Journal of Water and Health, 10, 1–10.CrossRefGoogle Scholar
  9. Gibbs, S. G., Green, C. F., Tarwater, P. M., Mota, L. C., Mena, K. D., & Scarpino, P. V. (2006). Isolation of antibiotic-resistant bacteria from the air plume downwind of a swine confined or concentrated animal feeding operation. Environmental Health Perspectives, 114, 1032–1037.CrossRefGoogle Scholar
  10. Gregova, G., Kmetova, M., Kmet, V., Venglovsky, J., & Feher, A. (2012). Antibiotic resistance of Escherichia coli isolated from a poultry slaughterhouse. Annals of Agricultural and Environmental Medicine, 19, 75–77.Google Scholar
  11. Heinonen-Tanski, H., Reponen, T., & Koivunen, J. (2009). Airborne enteric coliphages and bacteria in sewage treatment plants. Water Research, 43, 2558–2566.CrossRefGoogle Scholar
  12. Just, N. A., Letourneau, V., Kirychuk, S. P., Singh, B., & Duchaine, C. (2012). Potentially pathogenic bacteria and antimicrobial resistance in bioaerosols from cage-housed and floor-housed poultry operations. Annals of Occupational Hygiene, 56, 440–449.CrossRefGoogle Scholar
  13. Korzeniewska, E., Filipkowska, Z., Gotkowska-Plachta, A., Janczukowicz, W., Dixon, B., & Czulowska, M. (2009). Determination of emitted airborne microorganisms from a BIO-PAK wastewater treatment plant. Water Research, 43, 2841–2851.CrossRefGoogle Scholar
  14. Korzeniewska, E., Korzeniewska, A., & Harnisz, M. (2013). Antibiotic resistant Escherichia coli in hospital and municipal sewage and their emission to the environment. Ecotoxicology and Environment Safety, 91, 96–102.CrossRefGoogle Scholar
  15. Letourneau, V., Nehme, B., Meriaux, A., Masse, D., Cormier, Y., & Duchaine, C. (2010). Human pathogens and tetracycline-resistant bacteria in bioaerosols of swine confinement buildings and in nasal flora of hog producers. International Journal of Hygiene and Environmental Health, 213, 444–449.CrossRefGoogle Scholar
  16. Li, L., Gao, M., & Liu, J. (2011). Distribution characterization of microbial aerosols emitted from a wastewater treatment plant using the Orbal oxidation ditch process. Process Biochemistry, 46, 910–915.CrossRefGoogle Scholar
  17. Li, S., Zhao, M., Li, Y., Zhang, L., Zhang, X., & Miao, Z. (2013). Detection and source identification of airborne extended-spectrum beta-lactamase-producing Escherichia coli isolates in a chicken house. Aerobiologia, 29, 315–319.CrossRefGoogle Scholar
  18. Luczkiewicz, A., Jankowska, K., Fudala-Ksiazek, S., & Olanczuk-Neyman, K. (2010). Antimicrobial resistance of fecal indicators in municipal wastewater treatment plant. Water Research, 44, 5089–5097.CrossRefGoogle Scholar
  19. Magiorakos, A. P., Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., et al. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18, 268–281.CrossRefGoogle Scholar
  20. Nordmann, P., Naas, T., & Poirel, L. (2011). Global spread of Carbapenemase-producing Enterobacteriaceae. Emerging Infectious Diseases, 17, 1791–1798.CrossRefGoogle Scholar
  21. Paterson, D. L. (2006). Resistance in gram-negative bacteria: enterobacteriaceae. American Journal of Medicine, 119, S20–S28.CrossRefGoogle Scholar
  22. Pitout, J. D., & Laupland, K. B. (2008). Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infectious Diseases, 8, 159–166.CrossRefGoogle Scholar
  23. Reinthaler, F. F., Feierl, G., Galler, H., Haas, D., Leitner, E., Mascher, F., et al. (2010). ESBL-producing E. coli in Austrian sewage sludge. Water Research, 44, 1981–1985.CrossRefGoogle Scholar
  24. Sapkota, A. R., Ojo, K. K., Roberts, M. C., & Schwab, K. J. (2006). Antibiotic resistance genes in multidrug-resistant Enterococcus spp. and Streptococcus spp. recovered from the indoor air of a large-scale swine-feeding operation. Letters in Applied Microbiology, 43, 534–540.CrossRefGoogle Scholar
  25. Tao, R., Ying, G. G., Su, H. C., Zhou, H. W., & Sidhu, J. P. (2010). Detection of antibiotic resistance and tetracycline resistance genes in Enterobacteriaceae isolated from the Pearl rivers in South China. Environmental Pollution, 158, 2101–2109.CrossRefGoogle Scholar
  26. Teixeira, J. V., Miranda, S., Monteiro, R. A., Lopes, F. V., Madureira, J., Silva, G. V., et al. (2013). Assessment of indoor airborne contamination in a wastewater treatment plant. Environmental Monitoring and Assessment, 185, 59–72.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Juliana V. Teixeira
    • 1
  • Pedro Cecílio
    • 2
  • Daniela Gonçalves
    • 2
  • Vítor J. P. Vilar
    • 3
  • Eugénia Pinto
    • 1
    • 4
  • Helena N. Ferreira
    • 2
    Email author
  1. 1.CEQUIMED, Microbiology Service, Biological Sciences Department, Faculty of PharmacyUniversity of PortoPortoPortugal
  2. 2.REQUIMTE, Microbiology Service, Biological Sciences Department, Faculty of PharmacyUniversity of PortoPortoPortugal
  3. 3.LSRE—Laboratory of Separation and Reaction Engineering—Associate Laboratory LSRE/LCM, Faculty of EngineeringUniversity of PortoPortoPortugal
  4. 4.CIIMAR/CIMAR—Interdisciplinary Centre of Marine and Environmental ResearchUniversity of PortoPortoPortugal

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