Experimental Study of PhiX174 Resuspension from Mobile Bed Sediment
Publication: Journal of Irrigation and Drainage Engineering
Volume 147, Issue 5
Abstract
PhiX174 (or ) is a spherical single-stranded DNA bacteriophage used as a surrogate to study viral enteric pathogens in the environment. The resuspension of viral pathogen from bed sediment in irrigation canals impairs the quality of overlaying water and can result in the contamination of produce. We conducted a series of laboratory experiments to evaluate the resuspension of PhiX174 from bed sediment in an open channel flume. Different flow conditions (e.g., flow rate, velocity, shear stress) and three types of sediment mixtures (i.e., loam, sand, sandy loam) were investigated. Results revealed that the resuspension rate increases with the dimensionless bed shear stress. Based on these results, for the first time, we proposed two models to correlate the concentration of PhiX174 with the dimensionless bed shear stress for different sediment. One model was proposed for sandy loam and loam, was verified favorably by the experimental data, and yielded a Nash-Sutcliffe efficiency coefficient (NSE) of 0.71 and value of 0.72. The other model was proposed for sand, with NSE of 0.20 and of 0.26. The application of these models also indicated viruses are more easily resuspended from sand than sandy loam or loam sediments. The models shed a light for studying the correlation between the viruses in water and sediment and will benefit the management of irrigation water quality.
Get full access to this article
View all available purchase options and get full access to this article.
Data Availability Statement
All the data, including the experimental measurements, the data used for formulating empirical relations, and the code processing the data that support the findings of this study, are available from the corresponding author upon reasonable request.
Acknowledgments
The authors are grateful to The Center for Produce Safety for funding this research (Grant No. 2019CPS04). The authors would also like to acknowledge that any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of The Center for Produce Safety. Funding for this project was also made possible by the US Department of Agriculture’s Agricultural Marketing Service through grant USDA-AMS-TM-SCBGP-G-18-003 to the California Department of Food and Agriculture (Subaward: CDFA SCBGP#18-0275-079-SC). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the USDA. The Water and Energy Sustainable Technology (WEST) Center and the Hydraulic Laboratory at the University of Arizona provided in-kind support of laboratory facilities and supplies.
References
Abbaszadegan, M., M. Lechevallier, and C. Gerba. 2003. “Occurrence of viruses in US groundwaters.” J. Am. Water Works Assn. 95 (9): 107–120. https://doi.org/10.1002/j.1551-8833.2003.tb10458.x.
Adams, M. H. 1959. Bacteriophages. New York: Interscience Publishers.
Ashbolt, N. J., M. E. Schoen, J. A. Soller, and D. J. Roser. 2010. “Predicting pathogen risks to aid beach management: The real value of quantitative microbial risk assessment (QMRA).” Water Res. 44 (16): 4692–4703. https://doi.org/10.1016/j.watres.2010.06.048.
Bai, S., and W.-S. Lung. 2005. “Modeling sediment impact on the transport of fecal bacteria.” Water Res. 39 (20): 5232–5240. https://doi.org/10.1016/j.watres.2005.10.013.
Bitton, G., J. M. Davidson, and S. R. Farrah. 1979. “On the value of soil columns for assessing the transport pattern of viruses through soils: A critical outlook.” Water Air Soil Pollut. 12 (4): 449–457. https://doi.org/10.1007/BF01046866.
Black, K. S., T. J. Tolhurst, D. M. Paterson, and S. E. Hagerthey. 2002. “Working with natural cohesive sediments.” J. Hydraul. Eng. 128 (1): 2–8. https://doi.org/10.1061/(ASCE)0733-9429(2002)128:1(2).
Chandrasekaran, R., M. J. Hamilton, P. Wang, C. Staley, S. Matteson, A. Birr, and M. J. Sadowsky. 2015. “Geographic isolation of Escherichia coli genotypes in sediments and water of the Seven Mile Creek—A constructed riverine watershed.” Sci. Total Environ. 538 (Dec): 78–85. https://doi.org/10.1016/j.scitotenv.2015.08.013.
Cho, K. H., Y. A. Pachepsky, J. H. Kim, J.-W. Kim, and M.-H. Park. 2012. “The modified SWAT model for predicting fecal coliforms in the Wachusett Reservoir Watershed, USA.” Water Res. 46 (15): 4750–4760. https://doi.org/10.1016/j.watres.2012.05.057.
Colebrook, C. F., and C. M. White. 1937. “Experiments with fluid friction in roughened pipes.” Proc R Soc. London A 161 (906): 367–381. https://doi.org/10.1098/rspa.1937.0150.
Collins, R., and K. Rutherford. 2004. “Modelling bacterial water quality in streams draining pastoral land.” Water Res. 38 (3): 700–712. https://doi.org/10.1016/j.watres.2003.10.045.
Davies, C. M., J. A. Long, M. Donald, and N. J. Ashbolt. 1995. “Survival of fecal microorganisms in marine and freshwater sediments.” Appl. Environ. Microbiol. 61 (5): 1888–1896. https://doi.org/10.1128/AEM.61.5.1888-1896.1995.
de Brauwere, A., N. K. Ouattara, and P. Servais. 2014. “Modeling fecal indicator bacteria concentrations in natural surface waters: A review.” Crit. Rev. Environ. Sci. Technol. 44 (21): 2380–2453. https://doi.org/10.1080/10643389.2013.829978.
Dey, S. 2014. “Fluvial hydrodynamic.” In Hydrodynamic and sediment transport phenomena, 687. Berlin: Springer.
Duan, J. G., and S. Scott. 2007. “Selective bed-load transport in Las Vegas Wash, a gravel-bed stream.” J. Hydrol. 342 (3–4): 320–330. https://doi.org/10.1016/j.jhydrol.2007.06.001.
El Hadidy, A. M., S. Peldszus, and M. I. Van Dyke. 2013. “An evaluation of virus removal mechanisms by ultrafiltration membranes using MS2 and φX174 bacteriophage.” Sep. Purif. Technol. 120: 215–223.
Gall, A. M., B. J. Mariñas, Y. Lu, and J. L. Shisler. 2015. “Waterborne viruses: A barrier to safe drinking water.” PLoS Pathog. 11 (6): e1004867. https://doi.org/10.1371/journal.ppat.1004867.
García, M. H. 2008. “Sediment transport and morphodynamics.” In Sedimentation engineering: Processes, measurements, modeling, and practice, manuals and reports on engineering practice number 110, edited by M. H. García, 21–163. Reston, VA: ASCE.
Gerba, C. P., and D. Kayed. 2003. “Caliciviruses: A major cause of foodborne illness.” J. Food Sci. 68 (4): 1136–1137. https://doi.org/10.1111/j.1365-2621.2003.tb09614.x.
Gerba, C. P., and B. Keswick. 1981. “Survival and transport of enteric viruses and bacteria in groundwater.” Stud. Environ. Sci. 17: 511–515. https://doi.org/10.1016/S0166-1116(08)71944-7.
Gerba, C. P., and G. E. Schaiberger. 1975. “Effect of particulates on virus survival in seawater.” J. Water Pollut. Control Fed. 47 (1): 93–103.
Gil, M. I., M. V. Selma, T. Suslow, L. Jacxsens, M. Uyttendaele, and A. Allende. 2015. “Pre-and postharvest preventive measures and intervention strategies to control microbial food safety hazards of fresh leafy vegetables.” Crit. Rev. Food Sci. Nutr. 55 (4): 453–468. https://doi.org/10.1080/10408398.2012.657808.
Hassard, F., C. L. Gwyther, K. Farkas, A. Andrews, V. Jones, B. Cox, H. Brett, D. L. Jones, J. E. McDonald, and S. K. Malham. 2016. “Abundance and distribution of enteric bacteria and viruses in coastal and estuarine sediments—A review.” Front. Microbiol. 7 (Nov): 1692. https://doi.org/10.3389/fmicb.2016.01692.
Jamieson, R., D. M. Joy, H. Lee, R. Kostaschuk, and R. Gordon. 2005a. “Transport and deposition of sediment-associated Escherichia coli in natural streams.” Water Res. 39 (12): 2665–2675. https://doi.org/10.1016/j.watres.2005.04.040.
Jamieson, R. C., D. M. Joy, H. Lee, R. Kostaschuk, and R. J. Gordon. 2005b. “Resuspension of sediment-associated Escherichia coli in a natural stream.” J. Environ. Qual. 34 (2): 581–589. https://doi.org/10.2134/jeq2005.0581.
Jin, Y., and M. Flury. 2002. “Fate and transport of viruses in porous media.” Adv. Agron. 77 (1): 39–102. https://doi.org/10.1016/S0065-2113(02)77013-2.
Jurzik, L., I. A. Hamza, W. Puchert, K. Überla, and M. Wilhelm. 2010. “Chemical and microbiological parameters as possible indicators for human enteric viruses in surface water.” Int. J. Hyg. Environ. Health 213 (3): 210–216. https://doi.org/10.1016/j.ijheh.2010.05.005.
Karim, F. 1998. “Bed material discharge prediction for nonuniform bed sediments.” J. Hydraul. Eng. 124 (6): 597–604. https://doi.org/10.1061/(ASCE)0733-9429(1998)124:6(597).
Keswick, B. H., and C. P. Gerba. 1980. “Viruses in groundwater.” Environ. Sci. Technol. 14 (11): 1290–1297. https://doi.org/10.1021/es60171a602.
Kiaghadi, A., and H. S. Rifai. 2019. “Natural attenuation of indicator bacteria in coastal streams and estuarine environments.” Sci. Total Environ. 677 (Aug): 230–240. https://doi.org/10.1016/j.scitotenv.2019.04.315.
Kohn, T., and K. L. Nelson. 2007. “Sunlight-mediated inactivation of MS2 coliphage via exogenous singlet oxygen produced by sensitizers in natural waters.” Environ. Sci. Technol. 41 (1): 192–197. https://doi.org/10.1021/es061716i.
Kropinski, A. M., A. Mazzocco, T. E. Waddell, E. Lingohr, and R. P. Johnson. 2009. “Enumeration of bacteriophages by double agar overlay plaque assay.” In Bacteriophages: Methods and protocols. Volume 1: Isolation, characterization, and interactions, 69–76. Totowa, NJ: Humana Press.
Kunkel, E. A., C. V. Privette, C. B. Sawyer, and J. C. Hayes. 2013. “Attachment of Escherichia coli to fine sediment particles within construction sediment basins.” Adv. Biosci. Biotechnol. 4 (3): 407–414. https://doi.org/10.4236/abb.2013.43A054.
Lopman, B., P. Gastanaduy, G. W. Park, A. J. Hall, U. D. Parashar, and J. Vinjé. 2012. “Environmental transmission of norovirus gastroenteritis.” Curr. Opin. Virol. 2 (1): 96–102. https://doi.org/10.1016/j.coviro.2011.11.005.
Lytle, C. D., and L. B. Routson. 1995. “Minimized virus binding for tests of barrier materials.” Appl. Environ. Microbiol. 61 (2): 643–649. https://doi.org/10.1128/AEM.61.2.643-649.1995.
Marshall, K., and G. Bitton. 1980. “Microbial adhesion in perspective.” In Adsorption of microorganisms to surfaces, 1–5. New York: Wiley.
McKenna, R., D. Xia, P. Willingmann, L. L. IIag, S. Krishnaswamy, M. G. Rossmann, N. H. Olson, T. S. Baker, and N. L. Incardona. 1992. “Atomic structure of single-stranded DNA bacteriophage ΦX174 and its functional implications.” Nature 355 (6356): 137–143. https://doi.org/10.1038/355137a0.
Moriasi, D. N., J. G. Arnold, M. W. Van Liew, R. L. Bingner, R. D. Harmel, and T. L. Veith. 2007. “Model evaluation guidelines for systematic quantification of accuracy in watershed simulations.” Trans. ASABE 50 (3): 885–900. https://doi.org/10.13031/2013.23153.
Nash, J. E., and J. V. Sutcliffe. 1970. “River flow forecasting through conceptual models part I—A discussion of principles.” J. Hydrol. 10 (3): 282–290. https://doi.org/10.1016/0022-1694(70)90255-6.
Noonan, M., and J. McNabb. 1979. “Contamination of Canterbury groundwater by viruses.” In Quality and movement of groundwater in alluvial aquifers of New Zealand, 195–201. Lincoln, New Zealand: Dept. of Agricultural Microbiology Technical Publication, Lincoln College.
Olaimat, A. N., and R. A. Holley. 2012. “Factors influencing the microbial safety of fresh produce: A review.” Food Microbiol. 32 (1): 1–19. https://doi.org/10.1016/j.fm.2012.04.016.
Ouattara, N. K., A. de Brauwere, G. Billen, and P. Servais. 2013. “Modelling faecal contamination in the Scheldt drainage network.” J. Mar. Syst. 128 (Dec): 77–88. https://doi.org/10.1016/j.jmarsys.2012.05.004.
Pachepsky, Y., D. R. Shelton, J. E. McLain, J. Patel, and R. E. Mandrell. 2011. “Irrigation waters as a source of pathogenic microorganisms in produce: A review.” Adv. Agron. 113 (Jan): 75–141. https://doi.org/10.1016/B978-0-12-386473-4.00002-6.
Pandey, P. K., and M. L. Soupir. 2013. “Assessing the impacts of E. coli laden streambed sediment on E. coli loads over a range of flows and sediment characteristics.” J. Am. Water Resour. Assoc. 49 (6): 1261–1269. https://doi.org/10.1111/jawr.12079.
Piorkowski, G., R. Jamieson, G. Bezanson, L. T. Hansen, and C. Yost. 2013. “Evaluation of statistical models for predicting Escherichia coli particle attachment in fluvial systems.” Water Res. 47 (17): 6701–6711. https://doi.org/10.1016/j.watres.2013.09.003.
Quanrud, D. M., S. M. Carroll, C. P. Gerba, and R. G. Arnold. 2003. “Virus removal during simulated soil-aquifer treatment.” Water Res. 37 (4): 753–762. https://doi.org/10.1016/S0043-1354(02)00393-7.
Sanders, B. F., F. Arega, and M. Sutula. 2005. “Modeling the dry-weather tidal cycling of fecal indicator bacteria in surface waters of an intertidal wetland.” Water Res. 39 (14): 3394–3408. https://doi.org/10.1016/j.watres.2005.06.004.
Sassi, H. P., L. Y. Sifuentes, D. W. Koenig, E. Nichols, J. Clark-Greuel, L. F. Wong, K. McGrath, C. P. Gerba, and K. A. Reynolds. 2015. “Control of the spread of viruses in a long-term care facility using hygiene protocols.” Am. J. Infect. Control 43 (7): 702–706. https://doi.org/10.1016/j.ajic.2015.03.012.
Schijven, J. F., and S. M. Hassanizadeh. 2000. “Removal of viruses by soil passage: Overview of modeling, processes, and parameters.” Crit. Rev. Environ. Sci. Technol. 30 (1): 49–127. https://doi.org/10.1080/10643380091184174.
Scobey, F. C. 1939. Flow of water in irrigation and similar canals. Washington, DC: USDA, Div. Irrigation Bureau of Agricultural Engineering.
Shields, P., and S. Farrah. 1987. “Determination of the electrostatic and hydrophobic character of enteroviruses and bacteriophages.” In Proc., 87th Annual Meeting American Society of Microbiology. Washington, DC: American Society of Microbiology.
Stine, S. W., I. Song, C. Y. Choi, and C. P. Gerba. 2005. “Application of microbial risk assessment to the development of standards for enteric pathogens in water used to irrigate fresh produce.” J. Food Prot. 68 (5): 913–918. https://doi.org/10.4315/0362-028X-68.5.913.
Strauss, J. H., Jr., and R. L. Sinsheimer. 1963. “Purification and properties of bacteriophage MS2 and of its ribonucleic acid.” J. Mol. Biol. 7 (1): 43–54. https://doi.org/10.1016/S0022-2836(63)80017-0.
Terry, W. S. 2001. Open channel hydraulics. New York: McGraw-Hill.
Thilakarathne, M., V. Sridhar, and R. Karthikeyan. 2018. “Spatially explicit pollutant load-integrated in-stream E. coli concentration modeling in a mixed land-use catchment.” Water Res. 144 (Nov): 87–103. https://doi.org/10.1016/j.watres.2018.07.021.
Thompson, S. S., and M. V. Yates. 1999. “Bacteriophage inactivation at the air-water-solid interface in dynamic batch systems.” Appl. Environ. Microbiol. 65 (3): 1186–1190. https://doi.org/10.1128/AEM.65.3.1186-1190.1999.
Tian, Y. Q., P. Gong, J. D. Radke, and J. Scarborough. 2002. “Spatial and temporal modeling of microbial contaminants on grazing farmlands.” J. Environ. Qual. 31 (3): 860–869. https://doi.org/10.2134/jeq2002.8600.
USDA. 1987. Soil mechanics. Level I: Module 3—USDA textural soil classification, study guide. Washington, DC: National Soil Conservation Service.
USEPA. 1989. “National primary drinking water regulations: Filtration, disinfection; turbidity, Giardia Lamblia, viruses, Legionella and heterotrophic bacteria; final rule.” Fed. Regist. 54 (124): 27486.
Uyttendaele, M., L. A. Jaykus, P. Amoah, A. Chiodini, D. Cunliffe, L. Jacxsens, K. Holvoet, L. Korsten, M. Lau, and P. McClure. 2015. “Microbial hazards in irrigation water: Standards, norms, and testing to manage use of water in fresh produce primary production.” Compr. Rev. Food Sci. Food Saf. 14 (4): 336–356. https://doi.org/10.1111/1541-4337.12133.
Vanoni, V. A. 1975. Sedimentation engineering. New York: ASCE.
Wu, W., F. D. Shields Jr., S. J. Bennett, and S. S. Y. Wang. 2005. “A depth-averaged two-dimensional model for flow, sediment transport, and bed topography in curved channels with riparian vegetation.” Water Res. Res. 41 (3): W03015. https://doi.org/10.1029/2004WR003730.
Yakirevich, A., Y. Pachepsky, A. Guber, T. Gish, D. Shelton, and K. Cho. 2013. “Modeling transport of Escherichia coli in a creek during and after artificial high-flow events: Three-year study and analysis.” Water Res. 47 (8): 2676–2688. https://doi.org/10.1016/j.watres.2013.02.011.
Yang, C., and Y. Liu. 2017. “Simulation of the fate of faecal bacteria in estuarine and coastal waters based on a fractionated sediment transport model.” China Ocean Eng. 31 (4): 389–395. https://doi.org/10.1007/s13344-017-0045-y.
Zhang, H., J. Zhang, B. Zhao, and C. Zhang. 2010. “Removal of bacteriophages MS2 and phiX174 from aqueous solutions using a red soil.” J. Hazard. Mater. 180 (1–3): 640–647. https://doi.org/10.1016/j.jhazmat.2010.04.084.
Zhou, K., H. P. Sassi, C. M. Morrison, J. G. Duan, and C. P. Gerba. 2017. “Resuspension of Escherichia coli and MS2 bacteriophage from bed sediment in irrigation canals.” J. Irrig. Drain. Eng. 143 (6): 04017005. https://doi.org/10.1061/(ASCE)IR.1943-4774.0001169.
Information & Authors
Information
Published In
Copyright
© 2021 American Society of Civil Engineers.
History
Received: Mar 13, 2020
Accepted: Nov 25, 2020
Published online: Mar 4, 2021
Published in print: May 1, 2021
Discussion open until: Aug 4, 2021
Authors
Metrics & Citations
Metrics
Citations
Download citation
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.