DOI QR코드

DOI QR Code

Fate and Transport of Viruses in Soil and Groundwater Environments

토양.지하수 환경에서 바이러스의 거동

  • Park, Jeong-Ahn (Department of Rural Systems Engineering, Seoul National University) ;
  • Yoon, Seo-Young (Department of Rural Systems Engineering, Seoul National University) ;
  • Kim, Song-Bae (Department of Rural Systems Engineering, Seoul National University)
  • 박정안 (서울대학교 지역시스템공학과) ;
  • 윤서영 (서울대학교 지역시스템공학과) ;
  • 김성배 (서울대학교 지역시스템공학과)
  • Received : 2012.07.06
  • Accepted : 2012.07.27
  • Published : 2012.07.30

Abstract

Groundwater is widely used as drinking water supplies around the world. However, microbial contamination of groundwater is a serious environmental problem that degrades drinking water quality and poses a great threat to human health. Among the pathogenic microorganisms such as viruses, bacteria, and protozoa, viruses are not readily removed during transport through soils, having high mobility in groundwater environment due to their smaller size compared to bacteria and protozoa. Studies regarding the fate and transport of viruses in soils and aquifers are necessary to determine the vulnerability of groundwater to microbial contamination and to secure safe drinking water sources. Also, these studies provide important information to establish the regulations and policies related to public health. This review paper presented the field and laboratory studies conducted for the fate and transport of viruses in subsurface environments. Also, the paper provided the factors affecting the fate and transport of viruses, the characteristics of bacteriophages used for virus studies, and virus transport model/colloid filtration theory. Based on this review work, future researches should be performed actively to set up the viral protection zone for the protection of groundwater from viral contamination sources. Especially, the researches should be focused on the development of mathematical models to calculate the setback distance and travel time for the viral protection zone along with the accumulation of information related to the model parameters.

지하수는 전 세계적으로 널리 이용되는 음용수원이다. 하지만, 병원성 미생물에 의한 지하수 오염은 매우 심각한 환경문제로써 음용수의 수질을 저하시키고 인류의 건강을 위협한다. 지하수를 오염시키는 병원성 미생물은 바이러스, 세균, 원생동물 등이 있는데, 이중 바이러스는 박테리아나 원생동물보다 크기가 훨씬 작기 때문에 토양을 통과하는 과정에서 잘 제거되지 않고, 지하수 환경에서 이동성이 뛰어나다. 토양과 대수층에서 바이러스 거동 연구는 지하수의 병원성 미생물 오염 취약성을 판단하고 안전한 음용수원을 확보하는데 꼭 필요하다. 또한, 이러한 연구는 공중 보건을 위한 정책 및 규정을 제정하기 위한 중요한 정보를 제공한다. 본 논문에서는 최근까지의 지중 환경에서 바이러스 거동과 관련하여 수행된 연구들을 현장 조건에서 수행된 것과 실험실 조건에서 수행된 것으로 나눠 정리하였다. 또한, 이러한 연구들을 통해 알려진 바이러스의 거동에 영향을 미치는 인자들을 제시하였다. 그리고, 최근 바이러스 거동 연구에 널리 이용되는 박테리오파지의 특성을 정리하였고, 바이러스 거동을 모사하는데 이용되는 수학적 모델과 콜로이드 여과이론을 제시하였다. 지금까지의 연구결과를 바탕으로 향후 연구는 바이러스 오염원으로부터 지하수를 보호한다는 측면에서 바이러스 보호구역의 설정과 관련된 연구들이 활발히 진행되어야 할 것으로 판단된다. 특히, 바이러스 보호구역 설정과 관련하여 이격거리나 이동시간을 계산할 수 있는 수학적 모델을 개발하고 모델과 관련된 파라미터들의 정보를 축적하는데 집중되어야 할 것으로 판단된다.

Keywords

Acknowledgement

Supported by : 환경기술진흥원

References

  1. Schijven, J. F. and Hassanizadeh, S. M., "Removal of viruses by soil passage: overview of modeling, processes, and parameters," Crit. Rev. Environ. Sci. Technol., 30, 49-127(2000). https://doi.org/10.1080/10643380091184174
  2. Azadpour-Keeley, A. and Ward, C. H., "Transport and survival of viruses in the subsurface-processes, experiments, and simulation models," Remed. J., 15(3), 23-49(2005). https://doi.org/10.1002/rem.20048
  3. Van Cuyk, S. and Siegrist, R. L., "Virus removal within a soil infiltration zone as affected by effluent composition, application, and soil type," Water Res., 41, 699-709(1984).
  4. Nicosia, L. A., Rose, J. B., Stark, L. and Stewart, M. T., "A field study of virus removal in septic tank drainfields," J. Environ. Qual., 30, 1933-1939(2001). https://doi.org/10.2134/jeq2001.1933
  5. Bradford, S. A., Tadassa, Y. F. and Jin, Y., "Transport of coliphage in the presence and absence of manure suspension," J. Environ. Qual., 35, 1692-1701(2006). https://doi.org/10.2134/jeq2006.0036
  6. Horswell, J., Hewitt, J., Prosser, J., Van Schaik, A., Croucher, D., Macdonald, C., Burford, P., Susarla, P., Bickers, P. and Speir, T., "Mobility and survival of Salmonella typhimurium and human adenovirus from spiked sewage sludge applied to soil columns," J. Appl. Microbiol., 108, 104-114(2010). https://doi.org/10.1111/j.1365-2672.2009.04416.x
  7. Souter, P. F., Cruickshank, G. D., Tankerville, M. Z. Keswick, B. H., Ellis, B. D., Langworthy, D. E., Metz, K. A., Appleby, M. R., Hamilton, N., Jones, A. L. and Perry, J. D., "Evaluation of a new water treatment for point-of-use household applications to remove microorganisms and arsenic from drinking water," J. Water Health, 1, 73-84(2003).
  8. Kramer, M. N., Herwaldt, B. L., Craun, G. F., Calderone, R. L. and Juranek, D. D., "Waterborne disease: 1993 and 1994," J. Am. Water Works Assoc., 88, 66-80(1996).
  9. 환경부, 환경백서(2007).
  10. Bales, Roger C., Li, Shimin. and Yeh, T. C. J., "Bacteriophage and microsphere transport in saturated porous media: forced-gradient experiment at Borden, Ontario," Water Resour. Res., 33(4), 639-648(1997). https://doi.org/10.1029/97WR00025
  11. Deborde, D. C., Woessner, W. W., Kiley, Q. T. and Ball, P., "Rapid transport of viruses in a floodplain aquifer," Water Res., 33(10), 2229-2238(1999). https://doi.org/10.1016/S0043-1354(98)00450-3
  12. Ryan, J. N., Elimelech, M., Ard, R. A., Harvey, R. W. and Johnson, P. R., "Bacteriophage PRD1 and silica colloid transport and recovery in an iron oxide-coated sand aquifer," Environ. Sci. Technol., 33, 63-73(1999). https://doi.org/10.1021/es980350+
  13. Jansons, J., Edmonds, L. W., Speight, B. and Bucens, M. R., "Movement of viruses after artificial recharge," Water Res., 23(3), 293-299(1989). https://doi.org/10.1016/0043-1354(89)90094-8
  14. Wall, K., Pang, L., Sinton, L. and Close, M., "Transport and attenuation of microbial tracers and effluent microorganisms in saturated pumice sand aquifer material," Water Air Soil Pollut., 188, 213-224(2008). https://doi.org/10.1007/s11270-007-9537-3
  15. van der Wielen, P. W. J. J., Senden, W. J. M. K. and Medema, G., "Removal of bacteriophages MS2 and $\phi$X174 during transport in a sandy anoxic aquifer," Environ. Sci. Technol., 42, 4589-4594(2008). https://doi.org/10.1021/es800156c
  16. Flynn, R. M. and Sinreich, M., "Characterization of virus transport and attenuation in epikarst using short pulse and prolonged injection multi-tracer testing," Water Res., 44, 1138-1149(2010). https://doi.org/10.1016/j.watres.2009.11.032
  17. McKay, L. D., Harton, A. D. and Wilson, G. V., "Influence of flow rate on transport of bacteriophage in shale saprolite," Ground Water Qual., 31, 1095-1105(2002).
  18. Zhuang, J. and Jin, Y., "Virus retention and transport through Al-oxide coated sand columns: effects of ionic strength and composition," J. Contam. Hydrol., 60, 193-209(2003a). https://doi.org/10.1016/S0169-7722(02)00087-6
  19. Cheng, L., Chetochine, A. S., Pepper, I. L. and Brusseau, M. L., "Influence of DOC on MS-2 bacteriophage transport in a sandy soil," Water Air Soil Pollut., 178, 315-322(2007). https://doi.org/10.1007/s11270-006-9200-4
  20. Sadeghi, G., Schijven, J. F., Behrends, T., Hassanizadeh, S. M., Gerritse, J. and Kleingeld P. J., "Systematic study of effects of pH and ionic strength on attachment of Phage PRD1," Ground Water, 49(1), 12-19(2011). https://doi.org/10.1111/j.1745-6584.2010.00767.x
  21. Chu, Y., Jin, Y., Flury, M. and Yates, M. V., "Mechanisms of virus removal during transport in unsaturated porous media," Water Resour. Res., 37(2), 253-263(2001). https://doi.org/10.1029/2000WR900308
  22. Quanrud, D. M., Carroll, S. M., Gerba, C. P. and Arnold, R. G., "Virus removal during simulated soil-aquifer treatment," Water Res., 37, 753-762(2003). https://doi.org/10.1016/S0043-1354(02)00393-7
  23. Han, J., Jin, Y. and Wilson, C. S., "Virus retention and transport in chemically heterogeneous porous media under saturated and unsaturated flow conditions," Environ. Sci. Technol., 40, 1547-1555(2006). https://doi.org/10.1021/es051351m
  24. Torkzaban, S., Hassanizadeh, S. M., Schijven, J. F., de Bruin, H. A. M. and de Roda Husman, A. M., "Virus transport in saturated and unsaturated sand columns," Soil Sci. Soc. Am. J., 5(3), 877-885(2006).
  25. Kenst, A. B., Perfect, E., Wilhelm, S. W., Zhuang, J., Mc- Carthy, J. F. and Mckay, L. D., "Virus transport during infiltration of a wetting front into initially unsaturated sand columns," Environ. Sci. Technol., 42, 1102-1108(2008). https://doi.org/10.1021/es071213s
  26. Anders, R. and Chrysikopoulos, C. V., "Transport of viruses through saturated and unsaturated columns packed with sand," Trans. Porous Med., 76, 121-138(2009). https://doi.org/10.1007/s11242-008-9239-3
  27. Gerba, C. P., Sobsey, M. D., Wallis, C. and Melnick, J. L., "Adsorption of poliovirus onto activated carbon in wastewater," Environ. Sci. Technol., 9(8), 727-731(1975). https://doi.org/10.1021/es60106a009
  28. Bitton, G., Pancorbo, O. C., Overman, A. R. and Gifford, G. E., "Retention of viruses during sludge application to soils," Prog. Water Technol., 10, 597-606(1978).
  29. Moore, R. S., Taylor, D. H., Reddy, M. M. M. and Sturman, L. S., "Adsorption of reovirus by minerals and soils," Appl. Environ. Microbiol., 44(4), 852-859(1982).
  30. Yeager, J. G. and O'Brien, R. T., "Enterovirus inactivation in soil," Appl. Environ. Microbiol., 38(4), 963-975(1979).
  31. Sobsey, M. D., Dean, C. H., Knuckles, M. E. and Wagner, R. A., "Interactions and survival of enteric viruses in soil materials," Appl. Environ. Microbiol., 40, 92-101(1980).
  32. Moore, R. S., Taylor, D. H., Sturman, S. L., Reddy, M. M. and Fuhs, G. W., "Poliovirus adsorption by 34 minerals and soils," Appl. Environ. Microbiol., 42, 963-975(1981).
  33. Gerba, C. P. and Goyal, S. M., "Quantitative assessment of the adsorptive behavior of viruses to soils," Environ. Sci. Technol., 15, 940-944(1981). https://doi.org/10.1021/es00090a600
  34. Bales, R. C., Hinkle, S. R., Kroeger, T. W. and Stocking, K., "Bacteriophage adsorption during transport through porous media: chemical perturbations and reversibility," Environ. Sci. Technol., 25, 2088-2095(1991). https://doi.org/10.1021/es00024a016
  35. Kinoshita, T., Bales, R. C., Maguire, K. M. and Gerba, C. P., "Effect of pH on bacteriophage transport through sandy soils," J. Contam. Hydrol., 14, 55-70(1993). https://doi.org/10.1016/0169-7722(93)90041-P
  36. Burge, W. D. and Enkiri, N. K., "Virus adsorption by five soils," J. Environ. Qual., 7, 73-76(1978).
  37. Funderburg, S. W., Moore, B. E., Sagik, B. P. and Sorber, C. A., "Viral transport through soil columns under conditions of saturated flow," Water Res., 15, 703-711(1981). https://doi.org/10.1016/0043-1354(81)90163-9
  38. Fuhs, G. W. and Taylor, D. H., "Virus uptake by minerals and soils," In E. J. Middlebrooks (ed.) Water Reuse, Ann Arbor Sci. Pub., pp. 603-640(1982).
  39. Bitton, G., Scheuerman, P. R., Gifford, G. E. and Overman, A. R., "Laboratory studies on the movement of Poliovirus Type 1 through Cypress Dome soil," In K. C. Ewel and H. T. Odum (ed.) Cypress swamps. Univ. Presses of Florida, USA, pp. 216-224(1986).
  40. Jin, Y., Yates, M. V., Thompson, S. S. and Jury, W. A., "Sorption of viruses during flow through saturated sand columns," Environ. Sci. Technol., 31, 548-555(1997). https://doi.org/10.1021/es9604323
  41. Chu, Y., Jin, Y., Baumann, T. and Yates M. V., "Effect of soil properties on saturated and unsaturated virus transport through columns," J. Environ. Qual., 32, 2017-2025(2003). https://doi.org/10.2134/jeq2003.2017
  42. Dowd, S. E., Pillai, S. D., Wang, S. and Corapcioglu, M. Y., "Delineating the specific influence of virus adsorption and transport through sandy soils," Appl. Environ. Microbiol., 64, 450-410(1998).
  43. Goyal, S. M. and Gerba, C. P., "Comparative adsorption of human enteroviruses, simian rotavirus, and selected bacteriophages to soils," Appl. Environ. Microbiol., 38, 241-247 (1979).
  44. Gerba, C. P., Goyal, S. M., Cech, I. and Bogdan, G. F., "Quantitative assessment of the adsorptive behavior of viruses to soils," Environ. Sci. Technol., 15, 940-944(1981). https://doi.org/10.1021/es00090a600
  45. Gerba, C. P. and Bitton, G., "Microbial pollutants: their survival and transport pattern to groundwater," In Groundwater Pollut. Microbiol., New York, p. 78(1984).
  46. Lance, J. C. and Gerba, C. P., "Virus movement in soil during saturated and unsaturated flow," Appl. Environ. Microbiol., 47, 335-337(1984).
  47. Powelson, D. K. and Gerba, C. P., "Virus removal from sewage effluents during saturated and unsaturated flow through soil columns," Water Res., 28, 2175-2181(1994). https://doi.org/10.1016/0043-1354(94)90029-9
  48. Thomson, S. S. and Yates M. V., "Bacteriophage inactivation at the air-water-solid interface in dynamic batch systems," Appl. Environ. Microbiol., 65, 1186-1190(1999).
  49. Leclerc, H., Edberg, S., Pierzo, V. and Delattre, J. M., "Bacteriophages as indicators of enteric viruses and public health risk in groundwater," J. Appl. Microbiol., 88, 5-21(2000).
  50. Gerba, C. P., Powelson, D. K., Yahva, M. T., Wilson, L. G. and Amy, G. L., "Fate of viruses in treated sewage effluent during soil aquifer treatment designed for wastewater reclamation and reuse," Water Sci. Technol., 24(9), 95-102(1991).
  51. Attinti, R., Wei, J., Kniel, K., Sims, J. T. and Jin, Y., "Virus (MS2, $\phi$X174, and Aichi) attachment on sand measured by atomic force microscopy and their transport through sand columns," Environ. Sci. Technol., 44, 2426-2432(2010). https://doi.org/10.1021/es903221p
  52. Schijven, J. F., Hoogenboezem, W., Hassanizadeh, S. M. and Peters J. H., "Modeling removal of bacteriophages MS2 and PRD1 by dune recharge at Castricum, Netherlands," Water Resour. Res., 35(4), 1101-1111(1999). https://doi.org/10.1029/1998WR900108
  53. Schijven, J. F., Hassanizadeh, S. M., Dowd, S. E. and Pillai, S. D., "Modeling virus adsorption in batch and column experiments," Quantit. Microbiol., 2, 5-20(2000a). https://doi.org/10.1023/A:1010062728286
  54. Schijven, J. F., Medema, G., Vogelaar, A. J. and Hassanizadeh, S. M., "Removal of microorganisms by deep well injection," J. Contam. Hydrol., 44, 301-327(2000b). https://doi.org/10.1016/S0169-7722(00)00098-X
  55. Schijven, J. F. and Simunek, J., "Kinetic modeling of virus transport at the field scale," J. Contam. Hydrol., 55, 113- 135(2002). https://doi.org/10.1016/S0169-7722(01)00188-7
  56. Schijven, J. F., Hassanizadeh, S. M. and de Bruin, R. H. A. M., "Two-site kinetic modeling of bacteriophages transport through columns of saturated dune sand," J. Contam. Hydrol., 57, 259-279(2002). https://doi.org/10.1016/S0169-7722(01)00215-7
  57. Charles, K. J., Souter, F. C., Baker, D. L., Davies, C. M., Schijven, J. F., Roser, D. J., Deere, D. A., Priscott, P. K. and Ashbolt, N. J., "Fate and transport of viruses during sewage treatment in a mound system," Water Res., 42(12), 3047- 3056(2008). https://doi.org/10.1016/j.watres.2008.02.032
  58. Tufenkji, N. and Elimelech, M., "Correlation equation for predicting single-collector efficiency in physicochemical filtration in saturated porous media," Environ. Sci. Technol., 38(2), 529-536(2004). https://doi.org/10.1021/es034049r
  59. Blanford, W. J., Brusseaub, M. L., Yeh, T. C. J., Gerba, C. P. and Harvey, R., "Influence of water chemistry and travel distance on bacteriophage PRD-1 transport in a sandy aquifer," Water Res., 39, 2345-2357(2005). https://doi.org/10.1016/j.watres.2005.04.009
  60. Mallen, G., Maloszewski, P., Flynn, R., Rossi, P., Engel, M. and Seilerm K.-P., "Determination of bacterial and viral transport parameters in a gravel aquifer assuming linear kinetic sorption and desorption," J. Hydrol., 306, 21-36(2005). https://doi.org/10.1016/j.jhydrol.2004.08.033
  61. Pang, L., Close, M., Goltz, M., Noonan, M. and Sinton, L., "Filtration and transport of Bacillus subtilis spores and the F-RNA phage MS2 in a coarse alluvial gravel aquifer: Implications in the estimation of setback distances," J. Contam. Hydrol., 77, 165-194(2005). https://doi.org/10.1016/j.jconhyd.2004.12.006
  62. Weiss, W. J., Bouwer, E. J., Aboytes, R., LeChevallier, M. W., O'Melia, C. R., Le, B. T. and Schwab, K. J., "Riverbank filtration for control of microorganisms: results from field monitoring," Water Res., 39, 1990-2001(2005). https://doi.org/10.1016/j.watres.2005.03.018
  63. Flynn, R., Hunkeler, D., Guerin, C., Burn, C., Rossi, P. and Aragno, M., "Geochemical influences on H40/1 bacteriophage inactivation in glaciofluvial sands," Environ. Geol., 45, 504-517(2004). https://doi.org/10.1007/s00254-003-0905-z
  64. Pang, L., Close, M., Goltz, M., Sinton, L., Davies, H., Hall, C. and Stanton, G., "Estimation of septic tank setback distances based on transport of E. coli and F-RNA phages," Environ. Int., 29, 907-921(2003).
  65. Schulze-Makuch, D., Bowman, R. S., Pillai, S. D. and Guan, H., "Field evaluation of the effectiveness of surfactant modified zeolite and iron-oxide-coated sand for removing viruses and bacteria from ground water," Ground Water Monit. Remed., 23(4), 68-74(2003). https://doi.org/10.1111/j.1745-6592.2003.tb00696.x
  66. Ryan, J. N., Harvey, R. W., Metge, D., Elimelech, M., Navigato, T. and Pieper, A. P., "Field and laboratory investigations of inactivation of viruses (PRD1 and MS2) attached to iron oxide-coated quartz sand," Environ. Sci. Technol., 36, 2403-2413(2002). https://doi.org/10.1021/es011285y
  67. Woessner, W. W., Ball, P. N., DeBorde, D. C. and Troy, T. L., "Viral transport in a sand and gravel aquifer under field pumping conditions," Ground Water, 39(6), 886-894(2001). https://doi.org/10.1111/j.1745-6584.2001.tb02476.x
  68. Rossi, P., Dorfliger, N., Kennedy, K., Muller, I. and Aragno, M., "Bacteriophages as surface and ground water tracers," Hydrol. Earth Syst. Sci., 2(1), 101-110(1998). https://doi.org/10.5194/hess-2-101-1998
  69. Schijven, J. F., Hoogenboezem, W., Nobel, P. J., Medema, G. J. and Stakelbeek, A., "Reduction of FRNA-bacteriophages and faecal indicator bacteria by dune infiltration and estimation of sticking efficiencies," Water Sci. Technol., 38 (12), 127-131(1998).
  70. Pieper, A. P., Ryan, J. N., Harvey, R. W., Amy, G. L., Illangasekare, T. H. and Metge, D. W., "Transport and recovery of bacteriophage PRD1 in a sand and gravel aquifer: effect of sewage-derived organic matter," Environ. Sci. Technol., 31, 1163-1170(1997). https://doi.org/10.1021/es960670y
  71. Sinton, L. W., Finlay, R. K., Pang, L., Scott, D. M., "Transport of bacteria and bacteriophages in irrigated effluent into and through an alluvial gravel aquifer," Water Air Soil Pollut., 98, 17-42(1997).
  72. Bales, R. C., Li, S., Maguire, K. M., Yahya, M. T., Gerba, C. P. and Harvey, R. W., "Virus and bacteria transport in a sandy aquifer, Cape Cod, MA," Ground Water, 33(4), 653-661(1995). https://doi.org/10.1111/j.1745-6584.1995.tb00321.x
  73. Paul, J. H., Rose, J. B., Brown, J., Shinn, E. A., Miller, S. and Farrah, S. R., "Viral tracer studies indicate contamination of marine waters by sewage disposal practices in Key Largo, Florida," Appl. Environ. Microbiol., 61(6), 2230-2234 (1995).
  74. Mckay, L. D., Cherry, J. A., Bales, R. C., Yahya, M. T. and Gerba, C. P., "A field example of bacteriophage as tracers of fracture flow," Environ. Sci. Technol., 27, 1075-1079(1993). https://doi.org/10.1021/es00043a006
  75. Powelson, D. K., Gerba, C. P. and Yahya, M. T., "Virus tr ansport and removal in wastewater during aquifer recharge," Water Res., 27(4), 583-590(1993). https://doi.org/10.1016/0043-1354(93)90167-G
  76. Bales, R. C., Gerba, C. P., Grondin, G. H. and Jensen, S. L., "Bacteriophage transport in sandy soil and fractured tuff," Appl. Environ. Microbiol., 55(8), 2061-2067(1989).
  77. Bitton, G., Pancorbo, O. C. and Farrah, S. R., "Virus transport and survival after land application of sewage sludge," Appl. Environ. Microbiol., 47(5), 905-909(1984).
  78. Vaughn, J. M., Landry, E. F., Beckwith, C. A. and Thomas, M. Z., "Virus removal during groundwater recharge: effects of infiltration rate on adsorption of poliovirus to soil," Appl. Environ. Microbiol., 41(1), 139-147(1981).
  79. Damgaard-Larsen, S., Jensen, K. O., Lund, E. and Nissen, B., "Survival and movement of enterovirus in connection with land disposal of sludges," Water Res., 11(6), 503-508(1977). https://doi.org/10.1016/0043-1354(77)90037-9
  80. Martin, R. and Thomas, A., "An example of the use of bacteriophage as a groundwater tracer," J. Hydrol., 23, 73-78 (1974). https://doi.org/10.1016/0022-1694(74)90024-9
  81. Cao, H., Tsai, F. T.-C. and Rusch, K. A., "Salinity and soluble organic matter on virus sorption in sand and soil columns," Ground Water, 48(1), 42-52(2010). https://doi.org/10.1111/j.1745-6584.2009.00645.x
  82. Chrysikopoulos, C. V., Masciopinto, C., Mantia, R. L. and Manariotis. I. D., "Removal of biocolloids suspended in reclaimed wastewater by injection into a fractured aquifer model," Environ. Sci. Technol., 44, 971-977(2010). https://doi.org/10.1021/es902754n
  83. Sinton, L. W., Mackenzie, M. L., Karki, N., Braithwaithe, R. R., Hall, C. H. and Flintoft, M. J., "Transport of Escherichia coli and F-RNA bacteriophages in a 5 m column of saturated pea gravel," J. Contam. Hydrol., 117, 71-81(2010). https://doi.org/10.1016/j.jconhyd.2010.06.007
  84. Walshe, G. E., Pang, L., Flury, M., Close, M. E. and Flintoft, M., "Effects of pH, ionic strength, dissolved organic matter, and flow rate on the co-transport of MS2 bacteriophages with kaolinite in gravel aquifer media," Water Res., 44, 1255-1269(2010). https://doi.org/10.1016/j.watres.2009.11.034
  85. Aronino, R., Dlugy, C., Arkhangelsky, E., Shandalov, S., Oron, G., Brenner, A. and Gitis, V., "Removal of viruses from surface water and secondary effluents by sand filtration," Water Res., 43, 87-96(2009). https://doi.org/10.1016/j.watres.2008.10.036
  86. Cuyk, S. V. and Siegrist, R. L., "Virus removal within a soil infiltration zone as affected by effluent composition, application rate, and soil type," Water Res., 41, 699-709(2007). https://doi.org/10.1016/j.watres.2006.07.021
  87. Chetochine, A. S., Brusseau, M. L., Gerba, C. P. and Pepper, I. L., "Leaching of phage from class B biosolids and potential transport through soil," Appl. Environ. Microbiol., 72(1), 665-671(2006). https://doi.org/10.1128/AEM.72.1.665-671.2006
  88. Foppen, J. W. A., Okletey, S. and Schijven, J. F., "Effect of goethite coating and humic acid on the transport of bacteriophage PRD1 in columns of saturated sand," J. Contam. Hydrol., 85, 287-301(2006). https://doi.org/10.1016/j.jconhyd.2006.02.004
  89. Abudalo, R. A., Bogatsu, Y. G., Ryan, J. N., Harvey, R. W., Metge, D. W. and Elimelech, M., "Effect of ferric oxyhydroxide grain coatings on the transport of bacteriophage PRD1 and Cryptosporidium parvum Oocysts in the saturated porous media," Environ. Sci. Technol., 39, 6412-6419(2005). https://doi.org/10.1021/es050159h
  90. Assadian, N. W., Giovanni, G. D. D., Enciso, J., Iglesias, J. and Lindemann, W. "The transport of waterborne solutes and bacteriophage in soil subirrigated with a wastewater blend," Agric. Ecosyst. Environ., 111, 279-291(2005). https://doi.org/10.1016/j.agee.2005.05.010
  91. Keller, A. A. and Sirivithayapakorn, S., "Early breakthrough of colloids and bacteriophage MS2 in a water-saturated sand column," Water Resour. Res., 40, W08304(2004).
  92. Enriquez, C., Alum, A., Suarez-Rey, E. M., Choi, C. Y., Oron, G. and Gerba, C. P. "Bacteriophages MS2 and PRD1 in turfgrass by subsurface drip irrigation," J. Environ. Eng., 129(9), 852-857(2003). https://doi.org/10.1061/(ASCE)0733-9372(2003)129:9(852)
  93. Schijven, J. F., de Bruin, H. A. M., Hassanizadeh, S. M. and de Roda Husmana, A. M., "Bacteriophages and clostridium spores as indicator organisms for removal of pathogens by passage through saturated dune sand," Water Res., 37, 2186- 2194(2003). https://doi.org/10.1016/S0043-1354(02)00627-9
  94. Zhuang, J. and Jin, Y., "Virus retention and transport as influenced by different forms of soil organic matter," J. Environ. Qual., 32, 816-823(2003b). https://doi.org/10.2134/jeq2003.8160
  95. Cuyk, S. V., Siegrist, R., Logan, A., Masson, S., Fischer, E. and Figueroa, L., "Hydraulic and purification behaviors and their interactions during wastewater treatment in soil infiltration systems," Water Res., 35(4), 953-964(2001). https://doi.org/10.1016/S0043-1354(00)00349-3
  96. Carlander, A., Aronsson, P., Allestam, G., Stenström, T. A. and Perttu, K., "Transport and retention of bacterophages in two types of willow-cropped lysimeters," J. Environ. Sci. Health A, 35(8), 1477-1492(2000). https://doi.org/10.1080/10934520009377048
  97. Chu, Y., Jin, Y. and Yates, M. V., "Virus transport through saturated sand columns as affected by different buffer solutions," J. Environ. Qual., 29(4), 1103-1110(2000).
  98. Jin, Y., Pratt, E. and Yates, M. V., "Effect of mineral colloids on virus transport through saturated sand columns," J. Environ. Qual., 29, 532-539(2000a).
  99. Jin, Y., Chu, Y. and Li, Y., "Virus removal and transport in saturated and unsaturated sand columns," J. Contam. Hydrol., 43, 111-128(2000b). https://doi.org/10.1016/S0169-7722(00)00084-X
  100. Lukasik, J., Cheng, Y.-F., Lu, F., Tamplin, M. and Farrah, S. R., "Removal of microorganisms from water by columns containing sand coated with ferric and aluminum hydroxides," Water Res., 33(3), 769-777(1999). https://doi.org/10.1016/S0043-1354(98)00279-6
  101. Dowd, S. E. and Pillai, S. D., "Survival and transport of selected bacterial pathogens and indicator viruses under sandy aquifer conditions," J. Environ. Sci. Health A, 32(8), 2245- 2258(1997).
  102. Redman, J. A., Grant, S. B. and Olson, T. M., "Filtration of recombinant Norwalk virus particles and bacteriophage MS2 in quartz sand: importance of electrostatic interactions," Environ. Sci. Technol., 31, 3378-3383(1997). https://doi.org/10.1021/es961071u
  103. Loveland, J. P., Ryan, J. N., Amy, G. L. and Harvey, R. W., "The reversibility of virus attachment to mineral surfaces," Colloid Surf. A, 107, 205-221(1996). https://doi.org/10.1016/0927-7757(95)03373-4
  104. Penrod, S. L., Olson, T. M. and Grant, S. B., "Deposition kinetics of two viruses in packed beds of quartz granular media," Langmuir, 12, 5576-5587(1996). https://doi.org/10.1021/la950884d
  105. Poletika, N. N., Jury, W. A. and Yates, M. V., "Transport of bromide, simazine, and MS-2 coliphage in a lysimeter containing undisturbed, unsaturated soil," Water Resour. Res., 31 (4), 801-810(1995).
  106. Bales, R. C. and Li, S. "MS-2 and poliovirus transport in porous media: hydrophobic effects and chemical perturbations," Water Resour. Res., 29(4), 957-963(1993). https://doi.org/10.1029/92WR02986
  107. Herbold-Paschke, K., Straub, U., Hahn, T., Teutsch, G. and Botzenhart, K., "Behaviour of pathogenic bacteria, phages and viruses in groundwater during transport and adsorption," Water Sci. Technol., 24(2), 301-304(1991).
  108. Powelson, D. K., Simpson, J. R. and Gerba, C. P., "Effects of organic matter on virus transport in unsaturated flow," Appl. Environ. Microbiol., 57(8), 2192-2196(1991).
  109. Powelson, D. K., Simpson, J. R. and Gerba, C. P., "Virus transport and survival in saturated and unsaturated flow through soil columns," Ph. D. dissertation, University of Arizona (1990).
  110. Sobsey, M. D., Shields, P. A., Hauchman, F. H., Hazard, R. L. and Caton, L. W. "Survival and transport of hepatitis a virus in soils, groundwater and wastewater," Water Sci. Technol., 18(10), 97-106(1986).
  111. Landry, E. F., VaughN, J. M., Thomas, M. Z. and Beckwith, C. A., "Adsorption of enteroviruses to soil cores and their subsequent elution by artificial rainwater," Appl. Environ. Microbiol., 38(4), 680-687(1979).
  112. Gerba, C. P. and Lance, J. C., "Poliovirus removal from primary and secondary sewage effluent by soil filtration," Appl. Environ. Microbiol., 36(2), 247-251(1978).
  113. Lo, S. H. and Sproul, O, J., "Polio-virus adsorption from water onto silicate minerals," Water Res., 11, 653-658(1977). https://doi.org/10.1016/0043-1354(77)90103-8
  114. Lance, J. C., Gerba, C. P. and Melinick, J. L., "Virus movement in soil columns flooded with secondary sewage effluent," Appl. Environ. Microb., 32(4), 520-526(1976).
  115. Ackermann, H. W., "Bacteriophage classification. In: bacteriophages- biology and applications," eds. E. Kutter, A. Sulakvelidez. CRC Press, Boca Raton (2005).
  116. Arkhangelsky, E. and Gitis, V., "Effect of transmembrane pressure on rejection of viruses by ultrafiltration membranes," Sep. Purif. Technol., pp. 619-628(2008).