Skip to main content
Log in

Exposure to Airborne Noroviruses and Other Bioaerosol Components at a Wastewater Treatment Plant in Denmark

  • Original Paper
  • Published:
Food and Environmental Virology Aims and scope Submit manuscript

Abstract

Exposure to bioaerosols associated with wastewater treatment processes may represent an occupational health risk for workers at wastewater treatment plants (WWTPs). A high frequency of acute symptoms in the gastrointestinal tract among the wastewater workers at a Danish WWTP has been reported. The objective of the study was therefore to examine the exposure of the workers to aerosolised microorganisms. Sampling of inhalable endotoxin, bacteria, moulds and viruses was performed on one occasion using personal samplers. Noroviruses (NoVs) and endotoxin were detected at concentrations that could pose an occupational health risk and possibly contribute to the increased frequency of gastrointestinal illness among the workers and should therefore be investigated further. In addition, positive correlations between exposure to endotoxin, bacteria, moulds and NoVs were found and indicate that the exposure to bioaerosols may be related to work tasks. This is the first study directly showing an occupational exposure to airborne NoVs by its detection in airborne dust.

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

Similar content being viewed by others

References

  • Aizenberg, V., Grinshpun, S. A., Willeke, K., Smith, J., & Baron, P. A. (2000). Performance characteristics of the button personal inhalable aerosol sampler. AIHAJ, 61, 398–404.

    Article  PubMed  CAS  Google Scholar 

  • Boon, N., De Windt, W., Verstraete, W., & Top, E. M. (2002). Evaluation of nested PCR-DGGE (denaturing gradient gel electrophoresis) with group-specific 16S rRNA primers for the analysis of bacterial communities from different wastewater treatment plants. FEMS Microbiology and Ecology, 39, 101–112.

    CAS  Google Scholar 

  • Bünger, J., Antlauf-Lammers, M., Schulz, T. G., Westphal, G. A., Müller, M. M., Ruhnau, P., et al. (2000). Health complaints and immunological markers of exposure to bioaerosols among biowaste collectors and compost workers. Occupational and Environmental Medicine, 57, 458–464.

    Article  PubMed  Google Scholar 

  • Cheesbrough, J. S., Green, J., Gallimore, C. I., Wright, P. A., & Brown, D. W. G. (2000). Widespread environmental contamination with Norwalk-like viruses (NLV) detected in a prolonged hotel outbreak of gastroenteritis. Epidemiology and Infection, 125, 93–98.

    Article  PubMed  CAS  Google Scholar 

  • Clark, C. S. (1987). Potential and actual biological related health risks of wastewater industry employment. Journal of Water Pollution Control Federation, 59, 999–1008.

    CAS  Google Scholar 

  • Clark, C. S., Linnemann, J., & Gartside, P. S. (1985). Serologic survey of rotavirus, Norwalk agent and prototheca wickerhamii in wastewater workers. American Journal of Public Health, 75, 83–85.

    Article  PubMed  CAS  Google Scholar 

  • Clark, C. S., Rylander, R., & Larsson, L. (1983). Levels of gram-negative bacteria, Aspergillus fumigatus, dust, and endotoxin at compost plants. Applied and Environmental Microbiology, 45, 1501–1505.

    PubMed  CAS  Google Scholar 

  • Comelli, H. L., Rimstad, E., Larsen, S., & Myrmel, M. (2008). Detection of norovirus genotype I.3b and II.4 in bioaccumulated blue mussels using different virus recovery methods. International Journal of Food Microbiology, 127, 53–59.

    Article  PubMed  CAS  Google Scholar 

  • Costafreda, M. I., Bosch, A., & Rosa, M. (2006). Development, evaluation, and standardization of a real-time TaqMan reverse transcription-PCR assay for quantification of hepatitis A virus in clinical and shellfish samples. Applied and Environmental Microbiology, 72, 3846–3855.

    Article  PubMed  CAS  Google Scholar 

  • Da Silva, A. K., Le Saux, J. C., Parnaudeau, S., Pommepuy, M., Elimelech, M., & Le Guyader, F. (2007). Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: Different behaviors of genogroups I and II. Applied and Environmental Microbiology, 73, 7891–7897.

    Article  PubMed  CAS  Google Scholar 

  • Donham, K. J., Cumro, D., Reynolds, S. J., & Merchant, J. A. (2000). Dose-response relationships between occupational aerosol exposures and cross-shift declines of lung function in poultry workers: Recommendations for exposure limits. Journal of Occupational and Environmental Medicine, 42, 260–269.

    Article  PubMed  CAS  Google Scholar 

  • Douwes, J., Mannetje, A., & Heederik, D. (2001). Work-related symptoms in sewage treatment workers. Annals of Agricultural and Environmental Medicine, 8, 39–45.

    PubMed  CAS  Google Scholar 

  • Eduard, W. (2009). Fungal spores: A critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting. Critical Reviews in Toxicology, 39, 799–864.

    Article  PubMed  CAS  Google Scholar 

  • Gentry, J., Vinjé, J., & Lipp, E. K. (2009). A rapid and efficient method for quantitation of genogroups I and II norovirus from oysters and application in other complex environmental samples. Journal of Virological Methods, 156, 59–65.

    Article  PubMed  CAS  Google Scholar 

  • Grisoli, P., Rodolfi, M., Villani, S., Grignani, E., Cottica, D., Berri, A., et al. (2009). Assessment of airborne microorganism contamination in an industrial area characterized by an open composting facility and a wastewater treatment plant. Environmental Research, 109, 135–142.

    Article  PubMed  CAS  Google Scholar 

  • Haas, D., Unteregger, M., Habib, J., Galler, H., Marth, E., & Reinthaler, F. F. (2010). Exposure to Bioaerosol from sewage systems. Water, Air, and Soil pollution, 207, 49–56.

    Article  CAS  Google Scholar 

  • Haramoto, E., Katayama, H., Oguma, K., Ohgaki, S., Yamashita, H., Tajima, A., et al. (2006). Seasonal profiles of human noroviruses and indicator bacteria in a wastewater treatment plant in Tokyo, Japan. Water Science and Technology, 54, 301–308.

    Article  PubMed  CAS  Google Scholar 

  • Heinonen-Tanski, H., Reponen, T., & Koivunen, J. (2009). Airborne enteric coliphages and bacteria in sewage treatment plants. Water Research, 43, 2558–2566.

    Article  PubMed  CAS  Google Scholar 

  • Ivens, U. I., Breum, N. O., Ebbehoj, N., Nielsen, B. H., Poulsen, O. M., & Wurtz, H. (1999). Exposure-response relationship between gastrointestinal problems among waste collectors and bioaerosol exposure. Scandinavian Journal of Work, Environment and Health, 25, 238–245.

    PubMed  CAS  Google Scholar 

  • Jones, A. M., & Harrison, R. M. (2004). The effects of meteorological factors on atmospheric bioaerosol concentrations—A review. Science of the Total Environment, 326, 151–180.

    Article  PubMed  CAS  Google Scholar 

  • Jothikumar, N., Cromeans, T. L., Hill, V. R., Lu, X., Sobsey, M. D., & Erdman, D. D. (2005). Quantitative real-time PCR assays for detection of human adenoviruses and identification of serotypes 40 and 41. Applied and Environmental Microbiology, 71, 3131–3136.

    Article  PubMed  CAS  Google Scholar 

  • Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., et al. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of Clinical Microbiology, 41, 1548.

    Article  PubMed  CAS  Google Scholar 

  • Katayama, H., Haramoto, E., Oguma, K., Yamashita, H., Tajima, A., Nakajima, H., et al. (2008). One-year monthly quantitative survey of noroviruses, enteroviruses, and adenoviruses in wastewater collected from six plants in Japan. Water Research, 42, 1441–1448.

    Article  PubMed  CAS  Google Scholar 

  • Kenny, L. C., Aitken, R. J., Baldwin, P. E. J., Beaumont, G. C., & Maynard, A. D. (1999). The sampling efficiency of personal inhalable aerosol samplers in low air movement environments. Journal of Aerosol Science, 30, 627–638.

    Article  CAS  Google Scholar 

  • Kenny, L. C., Aitken, R., Chalmers, C., Fabriès, J. F., Gonzalez-Fernandez, E., Kromhout, H., et al. (1997). A collaborative European study of personal inhalable aerosol sampler performance. Annals of Occupational Hygiene, 41, 135–153.

    Article  PubMed  CAS  Google Scholar 

  • Kerr, S. M., Muranko, H. J., & Vincent, J. H. (2002). Personal sampling for inhalable aerosol exposures of carbon black manufacturing industry workers. Applied Occupational and Environmental Hygiene, 17, 681–692.

    Article  PubMed  CAS  Google Scholar 

  • Khuder, S. A., Arthur, T., Bisesi, M. S., & Schaub, E. A. (1998). Prevalence of infectious diseases and associated symptoms in wastewater treatment workers. American Journal of Industrial Medicine, 33, 571–577.

    Article  PubMed  CAS  Google Scholar 

  • Laitinen, S., Nevalainen, A., Kotimaa, M., Liesivuori, J., & Martikainen, P. J. (1992). Relationship between bacterial counts and endotoxin concentrations in the air of wastewater treatment plants. Applied and Environmental Microbiology, 58, 3774–3776.

    PubMed  CAS  Google Scholar 

  • Le Guyader, F., Parnaudeau, S., Schaeffer, J., Bosch, A., Loisy, F., Pommepuy, M., et al. (2009). Detection and quantification of noroviruses in shellfish. Applied and Environmental Microbiology, 75, 618–624.

    Article  PubMed  CAS  Google Scholar 

  • Loisy, F., Atmar, R. L., Guillon, P., Le Cann, P., Pommepuy, M., & Le Guyader, F. S. (2005). Real-time RT-PCR for norovirus screening in shellfish. Journal of Virological Methods, 123, 1–7.

    Article  PubMed  CAS  Google Scholar 

  • Lopman, B., Zambon, M., & Brown, D. W. (2008). The evolution of Norovirus, “the Gastric Flu”. PloS Medicine, 5, 187–189.

    Article  Google Scholar 

  • Lundholm, M., & Rylander, R. (1983). Work related symptoms among sewage workers. British Journal of Industrial Medicine, 40, 325–329.

    PubMed  CAS  Google Scholar 

  • Madsen, A. M. (2006a). Airborne endotoxin in different background environments and seasons. Annals of Agricultural and Environmental Medicine, 13, 81–86.

    PubMed  CAS  Google Scholar 

  • Madsen, A. M. (2006b). Exposure to airborne microbial components in autumn and spring during work at Danish biofuel plants. Annals of Occupational Hygiene, 50, 821–831.

    Article  PubMed  CAS  Google Scholar 

  • Madsen, A. M., & Sharma, A. K. (2008). Sampling of high amounts of bioaerosols using a high-volume electrostatic field sampler. Annals of Occupational Hygiene, 52, 167–176.

    Article  PubMed  CAS  Google Scholar 

  • Marks, P. J., Vipond, I. B., Carlisle, D., Deakin, D., Fey, R. E., & Caul, E. O. (2000). Evidence for airborne transmission of norwalk-like virus (NLV) in a hotel restaurant. Epidemiology and Infection, 124, 481–487.

    Article  PubMed  CAS  Google Scholar 

  • Marks, P. J., Vipond, I. B., Regan, F. M., Wedgwood, K., Fey, R. E., & Caul, E. O. (2003). A school outbreak of Norwalk-like virus: Evidence for airborne transmission. Epidemiology and Infection, 131, 727–736.

    Article  PubMed  CAS  Google Scholar 

  • Melbostad, E., Eduard, W., Skogstad, A., Sandven, P., Lassen, J., Sostrand, P., et al. (1994). Exposure to bacterial aerosols and work-related symptoms in sewage workers. American Journal of Industrial Medicine, 25, 59–63.

    Article  PubMed  CAS  Google Scholar 

  • Nielsen, E. M., Breum, N. O., Nielsen, B. H., Würtz, H., Poulsen, O. M., & Midtgaard, U. (1997). Bioaerosol exposure in waste collection: A comparative study on the significance of collection equipment, type of waste and seasonal variation. Annals of Occupational Hygiene, 41, 325–344.

    Article  CAS  Google Scholar 

  • Nordgren, J., Matussek, A., Mattsson, A., Svensson, L., & Lindgren, P. E. (2009). Prevalence of norovirus and factors influencing virus concentrations during one year in a full-scale wastewater treatment plant. Water Research, 43, 1117–1125.

    Article  PubMed  CAS  Google Scholar 

  • Oppliger, A., Duc, T. V., & Hilfiker, S. (2005). Influence of seasons and sampling strategy on assessment of bioaerosols in sewage treatment plants in Switzerland. Annals of Occupational Hygiene, 49, 393–400.

    Article  PubMed  CAS  Google Scholar 

  • Palmgren, U., Ström, G., Blomquist, G., & Malmberg, P. (1986). Collection of airborne microorganisms on nucleopore filters, estimation and analysis-CAMNEA method. Journal of Applied Bacteriology, 61, 401–406.

    Article  PubMed  CAS  Google Scholar 

  • Pepys, J., Jenkins, P. A., Festenstein, G. N., Gregory, P. H., Lacey, M. E., & Skinner, F. A. (1963). Farmer’s lung. Thermophilic actinomycetes as a source of “Farmer’s Lung Hay” antigen. Lancet, 2, 607–611.

    Article  PubMed  CAS  Google Scholar 

  • Rylander, R. (1999). Health effects among workers in sewage treatment plants. Occupational and Environmental Medicine, 56, 354–357.

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Monedero, M. A., Aguilar, M. I., Fenoll, R., & Roig, A. (2008). Effect of the aeration system on the levels of airborne microorganisms generated at wastewater treatment plants. Water Research, 42, 3739–3744.

    Article  PubMed  CAS  Google Scholar 

  • Schultz, A. C., Perelle, S., Di Pasquale, S., Kovac, K., De Medici, D., Fach, P., et al. (2011). Collaborative validation of a rapid method for efficient virus concentration in bottled water. International Journal of Food Microbiology, 145, 158–166.

    Article  Google Scholar 

  • Smit, L. A. M., Spaan, S., & Heederik, D. (2005). Endotoxin exposure and symptoms in wastewater treatment workers. American Journal of Industrial Medicine, 48, 30–39.

    Article  PubMed  Google Scholar 

  • Svraka, S., Duizer, E., Vennema, H., Bruin, E. D., Veer, B. V. D., Dorresteijn, B., et al. (2007). Etiological role of viruses in outbreaks of acute gastroenteritis in the Netherlands from 1994 through 2005. Journal of Clinical Microbiology, 45, 1389–1394.

    Article  PubMed  Google Scholar 

  • Teunis, P. F. M., Moe, C. L., Liu, P., Miller, S. E., Lindesmith, L., Baric, R. S., et al. (2008). Norwalk virus: How infectious is it? Journal of Medical Virology, 80, 1468–1476.

    Article  PubMed  Google Scholar 

  • Thorn, J., Beijer, L., & Rylander, R. (2002). Work related symptoms among sewage workers: A nationwide survey in Sweden. Occupational and Environmental Medicine, 59, 562–566.

    Article  PubMed  CAS  Google Scholar 

  • Uhrbrand, K., Myrmel, M., Maunula, L., Vainio, K., Trebbien, R., Nørrung, B., et al. (2010). Evaluation of a rapid method for recovery of norovirus and hepatitis A virus from oysters and blue mussels. Journal of Virological Methods, 169, 70–78.

    Article  PubMed  CAS  Google Scholar 

  • Van Hooste, W., Charlier, A. M., Rotsaert, P., Bulterys, S., Moens, G., van Sprundel, M., et al. (2010). Work-related Helicobacter pylori infection among sewage workers in municipal wastewater treatment plants in Belgium. Occupational and Environmental Medicine, 67, 91–97.

    Article  PubMed  Google Scholar 

  • Vinjé, J. (2010). A Norovirus vaccine on the horizon? Journal of Infectious Diseases, 202, 1623–1625.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The work was partially supported by grant NKJ-130 from the Nordic Joint Committee for Agricultural Research. We highly acknowledged Thora Brendstrup and Birgitte Zwicky-Hauschild at Occupational Health Consultancy, City of Copenhagen, as well as Albert Dam for initiating this study. We thank Margit W. Frederiksen for skilful technical assistance and the WWTP workers for their participation in the project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katrine Uhrbrand.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Uhrbrand, K., Schultz, A.C. & Madsen, A.M. Exposure to Airborne Noroviruses and Other Bioaerosol Components at a Wastewater Treatment Plant in Denmark. Food Environ Virol 3, 130–137 (2011). https://doi.org/10.1007/s12560-011-9068-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12560-011-9068-3

Keywords

Navigation