Abstract
Bacteriophages MS-2 and PRD-1 were used as indicators of human viral behaviour in a series of turf-grass irrigation and washing machine experiments to provide information about the level of human exposure to potential residual enteric viruses in recycled water that can affect health. Results provided evidence to support a potential inadvertent exposure volume of 0.01 ml for recycled water used for machine clothes washing. Results for irrigation experiments showed that a one log reduction in bacteriophage numbers on turf-grass was not achieved under exposure to high solar conditions after 4 h. Experimentation showed that bacteriophages may be usefully employed in exposure assessment studies based on the ease of their enumeration and logistical and cost considerations. In terms of future studies, observed differences in individual bacteriophage characteristics provide a rationale for using multiple viral indicators. However, limitations on the utility of bacteriophage also need to be considered.
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References
Adams, M. H. (1959). Bacteriophages. New York: Interscience Publishers, Inc.
Allwood, P. B., Malik, Y. S., Hedberg, C. W., & Goyal, S. M. (2004). Effect of temperature and sanitizers on the survival of feline calicivirus, Escherichia coli, and F-specific coliphage MS2 on leafy salad vegetables. Journal of Food Protection, 67, 1451–1456.
Alonso, M. C., Dionisio, L. P. C., Bosch, A., De Moura, B. S., Garcia-Rosado, E., & Borrego, J. J. (2006). Microbiological quality of reclaimed water used for golf courses’ irrigation. Water Science and Technology, 54, 109–117.
Badawy, A. S., Rose, J. B., & Gerba, C. P. (1990). Comparative survival of enteric viruses and coliphage on sewage irrigated grass. Journal of Environmental Science and Health, A25, 937–952.
Brooks, J. P., Tanner, B. D., Gerba, C. P., Haas, C. N., & Pepper, I. L. (2004). Estimation of bioaerosol risk of infection to residents adjacent to land applied biosolids site using an empirically derived transport model. Journal of Applied Microbiology, 50, 7–12.
Corapcioglu, M. Y., Vogel, J. R., Munster, C. L., Pillai, S. D., Dowd, S., & Wang, S. (2006). Virus transport experiments in a sandy aquifer. Water, Air, and Soil Pollution, 169, 47–65.
CRCWQT. (2008). Study of water usage in urban areas. Research report No. 53. Adelaide, Cooperative Research Centre for Water Quality & Treatment.
Dawson, D. J., Paish, A., Staffell, L. M., Seymour, I. J., & Appleton, H. (2005). Survival of viruses on fresh produce, using MS2 as a surrogate for norovirus. Journal of Applied Microbiology, 98, 203–209.
Doré, W. J., Henshilwood, K., & Lees, D. N. (2000). Evaluation of F-specific RNA bacteriophage as a candidate human enteric virus indicator for bivalve molluscan shellfish. Applied and Environmental Microbiology, 66, 1280–1285.
Dowd, S., Pillai, S. D., Wang, S., & Corapcioglu, M. Y. (1998). Delineating the specific influence of virus isoelectric point and size on virus adsorption and transport through sandy soils. Applied and Environmental Microbiology, 64, 405–410.
Drees, K. P., Abbaszadegan, M., & Maier, R. M. (2003). Comparative electrochemical inactivation of bacteria and bacteriophage. Water Research, 37, 2291–2300.
Durán, A. E., Muniesa, M., Mocé-Llivina, L., Campos, C., Jofre, J., & Lucena, F. (2003). Usefulness of different groups of bacteriophages as model micro-organisms for evaluating chlorination. Journal of Applied Microbiology, 95, 29–37.
Enriquez, C., Alum, A., Suarez-Rey, E. M., Choi, C. Y., Oron, G., & Gerba, C. P. (2003). Bacteriophages MS2 and PRD1 in turfgrass by subsurface drip irrigation. Journal of Environmental Engineering, 129, 852–857.
Gerba, C. P., & Kennedy, D. (2007). Enteric virus survival during household laundering and impact of disinfection with sodium hypochlorite. Applied and Environmental Microbiology, 73, 4425–4428.
Girones, R. (2006). Tracking viruses that contaminate environments. Microbe, 1, 19–25.
Harvey, R. W., & Ryan, J. N. (2004). Use of PRDI bacteriophage in groundwater viral transport, inactivation, and attachment studies. FEMS Microbiology Ecology, 49, 3–16.
NRMMC/EPHC/AHMC. (2006). National Water Quality Management Strategy-Australian Guidelines for Water Recycling: Managing Health and Environmental Risks (Phase 1). National Resource Management Ministerial Council, Environmental Protection and Heritage Council and Australian Health Ministers Conference.
O’Connell, K. P., Bucher, J. R., Anderson, P. E., Cao, C. J., Khan, A. S., Gostomski, M. V., et al. (2006). Real-time fluorogenic reverse transcription-PCR assays for detection of bacteriophage MS2. Applied and Environmental Microbiology, 72, 478–483.
O’Toole, J., Sinclair, M., Diaper, C., & Leder, K. (2008). Comparative survival of enteric indicators, E. coli and somatic and F-RNA bacteriophages on turf-grass irrigated with recycled water. Water Science and Technology, 58, 513–518.
PMSEIC. (2007). Water for our cities: building resilience in a climate of uncertainty—A report of the PMSEIC (Prime Minister’s Science, Engineering and Innovation Council) working group. Canberra: Australian Government.
Rusin, P., Maxwell, S., & Gerba, C. (2002). Comparative surface-to-hand and fingertip-to-mouth transfer efficiency of gram-positive, gram-negative bacteria, and phage. Journal of Applied Microbiology, 93, 585–592.
Ryan, J. N., Harvey, R. W., Metge, D., Elimelech, M., Navigato, T., & Pieper, A. P. (2002). Field and laboratory investigations of inactivation of viruses (PRD1 and MS2) attached to iron oxide-coated quartz sand. Environmental Science and Technology, 36, 2403–2413.
Schijven, J. F., De Bruin, H. A. M., Hassanizadeh, S. M., & De Roda Husman, A. M. (2003). Bacteriophages and Clostridium spores as indicator organisms for removal of pathogens by passage through saturated dune sand. Water Research, 37, 2186–2194.
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The authors wish to thank Naomi Cooke for her technical assistance. Funding from the Cooperative Research Centre for Water Quality and Treatment, Australia; Australian National Health and Medical Research Council and the Victorian Water Trust is acknowledged.
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O’Toole, J.E., Sinclair, M.I. & Leder, K. Using Bacteriophages in Recycled Water Exposure Assessment Studies. Food Environ Virol 1, 23–30 (2009). https://doi.org/10.1007/s12560-008-9003-4
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DOI: https://doi.org/10.1007/s12560-008-9003-4