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a Department of Plant and Soil Sciences, University of Delaware, Newark, DE 19717
b Institute of Hydrochemistry, Technical University of Munich, Marchioninistrasse 17, D-81377, Munich, Germany
c Y. Chu, current address), Department of Environmental Sciences, University of California, Riverside, CA 92521
* Corresponding author (yjin{at}udel.edu).
Received for publication August 6, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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X174 and MS-2, and Br- tracer in a phosphate-buffered saline solution were introduced into saturated and unsaturated soil columns as a step function under constant flow rate and hydraulic conditions. Results showed that significantly greater virus removal occurred in the unsaturated columns than in the saturated columns in the two soils containing high metal oxides content. However, the increase in virus retention under unsaturated conditions was not significant in two other soils having high phosphorus and calcium contents and high pH, and in another soil with high organic matter content. The results imply that the extent of water content effect on inactivation and sorption of viruses can range from significant to minimal depending on the properties of the transport medium. We found that the presence of in situ metal oxides was a significant factor responsible for virus sorption and inactivation. Therefore, soils with high metal oxides content may have the potential to be used as hydrological barriers in preventing microbial contamination in the subsurface environments. We also found that the water content effect on virus removal and inactivation strongly depended on solid properties of the testing medium.
Abbreviations: OM, organic matter
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Researchers have made many attempts at identifying soil properties that affect virus sorption. In studying virus sorption by five soils, Burge and Enkiri (1978a) found that when virus sorption rates were plotted against cation exchange capacity, specific surface area, and organic matter (OM) content, good correlations existed for four of the soils. The lack of correlation for the fifth soil might have resulted from its high OM content, which blocked sites for virus sorption. Goyal and Gerba (1979) reported that among several soil characteristics including texture, OM content, soil pH, resin-extractable phosphorus (P), total Al, and exchangeable Al contents, soil pH was the most significant factor affecting virus sorption. Moore et al. (1981) studied poliovirus sorption by 34 minerals and soils and found that montmorillonite, glauconite, and bituminous shale were the least effective. Magnetite sand and hematite, which are predominantly iron (Fe) oxides, were the most effective. Gerba et al. (1981) showed that for viruses that are sensitive to soil properties, the most important factors affecting their sorption were pH, OM, and exchangeable Fe content of the soil. Moore et al. (1982) investigated reovirus sorption by 30 soils, minerals, and rocks, and found that sorption increased with the presence of divalent cations and increasing surface area.
The degree of water saturation has been found to have significant effects on virus transport through porous media due to enhanced virus sorption or inactivation during unsaturated transport. Sobsey et al. (1980) found that although sandy and organic soil materials were poor adsorbents for poliovirus when suspended in wastewater, they removed at least 95% of viruses from intermittently applied wastewater through unsaturated columns. Lance and Gerba (1984) found that movement of poliovirus during unsaturated flow of sewage through soil columns was much less than during saturated flow. Powelson et al. (1990) reported that under saturated conditions MS-2 bacteriophage showed little sorption or inactivation by a loamy fine sand, while under unsaturated conditions MS-2 was strongly removed from the soil water. In another column study, Powelson and Gerba (1994) showed that unsaturated flow of sewage effluents removed MS-2, PRD1, and poliovirus more than three times compared with saturated flow in a sandy alluvium soil.
Though the effects of water content on virus inactivation have been well documented, more detailed information such as the extent of virus retention caused by unsaturated conditions and its relationship with other factors remains unknown. Previous studies on identification of soil characteristics affecting virus removal were conducted either in batch experiments or under saturated flow conditions. It remains unclear how soil properties interactively affect virus removal during transport under unsaturated conditions.
This study was designed to use a well-controlled column system in which the water content was kept uniform and flow at a steady state. The goal of this study was to assess virus behavior in several representative soils or aquifer materials found around the United States. The specific objectives were to (i) investigate the water content effect on virus transport through columns packed with selected soils having different properties and (ii) evaluate the key factors that control virus transport in real soils under both saturated and unsaturated water flow conditions.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Viruses and Viral Assay
Two bacteriophages, MS-2 and X174, were used as model viruses in this study. These organisms were chosen because of their structural resemblance to many human enteric viruses and because they have been studied as surrogates for human enteric viruses in numerous investigations. Bacteriophage MS-2 is an icosahedral single-stranded (linear) RNA phage with a diameter of 26.0 to 26.6 nm (Vanduin, 1988) and an isoelectric point of 3.9 (Zerda, 1982). It is grown on bacterial lawns of Escherichia coli from the American Type Culture Collection (ATCC 15597). Bacteriophage X174 is a spherical single-stranded (circular) DNA bacteriophage, approximately 23 nm in diameter with an isoelectric point of 6.6 (Ackerman and Dubow, 1987). It is grown on its host E. coli (ATCC 13706).
Both X174 and MS-2 bacteriophages were assayed by the double-agar overlay method described by Adams (1959) with the aforementioned bacterial hosts. One milliliter of log-phase E. coli host and 1.0 or 0.1 mL of sample were combined and mixed in a tube of molten tryptic soy agar (TSA; Difco Laboratories, Detroit, MI) and poured onto TSA plates. The plates were then incubated at 37°C overnight for MS-2 and 5 h for X174, respectively. Samples were plated in duplicate and each reported virus concentration was determined by averaging the number of plaques from two replicate plates. Only the dilutions that resulted in 30 to 300 plaques per plate were considered countable.
Experimental Setup
The column apparatus and procedures for conducting saturated and unsaturated experiments are the same as previously reported (Jin et al., 2000a; Chu et al., 2001). Only a brief description of the experimental setup is given here. The saturated system consisted of a 10-cm-long, 7.6-cm-diameter column with a top and bottom plate, all made of acrylate. The system was sealed with an O-ring on each end (the O-rings had no contact with the interior of the column). The apparatus for the unsaturated column had an additional solution-filling column positioned on top of the transport column. Seventeen syringe needles were evenly distributed on the bottom of the solution-filling column to ensure uniform supply of the input solution. A stainless steel porous plate (3.175 mm thick) with a pore size of 0.5 µm and a bubbling pressure of 10.1 to 13.5 kPa (Mott Industrial, Farmington, CT) was placed at the bottom of the column. The column outlet was connected to a vacuum chamber with a fraction collector inside. Adjusting the vacuum pressure and flow rate of the input solution achieved a steady state flow rate, as well as essentially uniform water contents in all experiments. Two small stainless steel tensiometers (diameter 0.56 cm) were installed at depths of 3.3 and 6.6 cm to monitor water potentials to verify that the columns indeed had a uniform water distribution. The tensiometers were connected to electronic pressure transducers and electrical voltage readings were collected intermittently during the experiment. The voltage readings were transferred to matric potential values using linear calibration curves obtained separately by hanging columns (r2 = 0.9999).
Virus Transport Experiments
All experiments were conducted under steady state flow conditions. Tensiometer readings recorded during each experiment showed that the measurements at the two locations reached similar or identical values (maximum deviation of matric potential as indicated by tensiometer readings from averaged values was 4%), indicating that water distribution was essentially uniform. The averaged matric potential values for each soil are listed in Table 3.
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X174 was introduced into soil columns as a step function. To recover viable viruses reversibly sorbed by soil particles during transport, beef extract 3% solution (pH 9.5) was used to desorb viruses from the columns when retention was observed. Table 3 lists selected experimental parameters. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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X174 Transport through Columns Packed with Delaware 1 and 2X174. For example, in Delaware 1 at approximately 10 pore volumes, the C/C0 (ratio of outflow concentration to input concentration) at 100% saturation was 1000 times greater for MS-2 and 1.8 times greater for X174 than the C/C0 values at 66% saturation. The results obtained from experiments with Delaware 2 were similar to those obtained in Delaware 1, except that more virus retention was observed and the final C/C0 values for MS-2 were even lower in Delaware 2 than in Delaware 1.
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X174 Transport through Columns Packed with California, Arizona, and Georgia SoilsX174 in all soils and for MS-2 in the Arizona and Georgia soils. MS-2 removal was greater at the lower water content in the California soil; however, the extent of the water content effect was much smaller than that observed in the two Delaware soils. For both viruses, more viral removal was observed in the California soil than in the Arizona and Georgia soils.
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X174 could be recovered from the saturated columns than from the unsaturated columns. As a general trend, low percentages of the retained MS-2 were recovered by beef extract solution in all soils from both saturated and unsaturated experiments, indicating that more MS-2 might have been inactivated, or irreversibly sorbed, or both, during unsaturated transport. In one exception to the general trend, the MS-2 recovery in saturated Delaware 2 was extremely low as compared with the other soils. This might be caused by sorption onto and subsequent inactivation by metal oxides. Elution experiments were not conducted for the Georgia soil.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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X174 in saturated California soil column. The Delaware soils have much higher citrate–dithionite-extracted Fe (identified by TGA analysis as mainly goethite) content than the other soils (Table 1). This suggests that the metal oxides on the surfaces of the Delaware soils may be responsible for the high extent of virus removal in these two soils. Similar effects of metal oxides on virus retention have been reported in batch experiments (Murray and Laband, 1979; Moore et al., 1981; Gerba et al., 1981) and in column and field experiments (Pieper et al., 1997; Chu et al., 2001; Ryan et al., 2002). Chu et al. (2001) used a nonreactive (metal oxides removed) and a reactive (pure sand coated with goethite) sand to investigate the effect of iron oxides on the retention and transport of MS-2 and X174 under saturated and unsaturated flow conditions. Their experimental data clearly showed that the presence of goethite dominated the removal of the viruses over the effect of unsaturated flow. These results suggest that soils with high metal oxide content could be considered as hydrological barriers, or as materials for a reactive barrier wall, that could prevent the movement of viruses.
Surface Area
Larger specific surface area associated with the two Delaware soils could be another reason that more viruses were removed during transport in Delaware 1 and 2 than in the California, Arizona, and Georgia soils. Similarly, Delaware 2 removed more viruses than Delaware 1 because Delaware 2 contains a much higher percentage of finer sand particles than Delaware 1, meaning that it has a larger specific surface area (Table 1).
Clay Minerals
Studies have shown that soils with high clay content have a high sorption capacity for viruses (Gerba et al., 1975; Bitton et al., 1978). The association of viruses with clay minerals has been attributed to the large surface area and high cation exchange capacity (CEC) of clays. The mechanisms and sites of sorption differ for different viruses and are influenced by characteristics of the clays such as anion exchange capacity (AEC), CEC, and AEC to CEC ratios (Schiffenbauer and Stotzky, 1982). Both positively and negatively charged sites on clay minerals are involved in virus sorption. Lipson and Stotzky (1983)( 1985) found that reovirus was sorbed more onto montmorillonite than onto kaolinite. Schiffenbauer and Stotzky (1982) showed that maximum sorption of coliphages T7 and T1 was greater by kaolinite than by montmorillonite. Moore et al. (1981) observed that montmorillonite was one of the least effective minerals in virus sorption. Insufficient information is available from the current study to differentiate the effect between smectite (the major clay mineral in California and Arizona soils) and kaolinite (the major clay mineral in the Delaware soils) on the observed virus behavior.
Suspended Particles
Cloudiness indicating release of suspended particles from the soils was observed in many outflow samples, especially those collected at the initial stage of the experiments. Subsequent analysis with a scanning electron microscope (SEM) confirmed that suspending mineral colloids were present in solution samples. It was possible that viruses were sorbed on the suspending colloids and subsequently transported through the columns. Jin et al. (2000b) found that the Na-montmorillonite greatly enhanced MS-2 transport through the sand columns. Conceivably, suspended particles could adsorb viruses and facilitate their transport. The higher outflow concentration of viruses in the Arizona soil than in the California soil is consistent with the Arizona soil's higher clay content (Table 1).
Phosphorus and Calcium Contents
Yates et al. (1985) found that the concentration of Ca in 11 ground water samples was significantly correlated with the inactivation rate of MS-2: as the Ca concentration increased, the inactivation rate increased. Carlson et al. (1968) demonstrated that sorption of bacteriophage T2 onto suspended clay materials was positively correlated with Ca concentrations, and proposed that polyvalent cations in the environment serve as bridges between anionic groups on a virus and negatively charged sites on clay. Burge and Enkiri (1978b) found that sorption rate of X174 was higher for the Ca-saturated soil than the untreated soil. Goyal and Gerba (1979) demonstrated significantly increased virus sorption when Ca levels were increased from 0.001 to 0.01 M CaCl2. Lipson and Stotzky (1983) found that the sequence of the amount of adsorption to homoionic montmorillonite was Al > Ca > Mg > Na > K; the sequence of sorption to kaolinite was Na > Al > Ca > Mg > K. However, compared with the other soil properties, P and Ca content did not significantly affect virus sorption (Gerba et al., 1981). Moore et al. (1981) found similar results, observing that the elemental composition of the sorbents had little effect on poliovirus uptake. In this study, the high P and Ca contents that characterized the California and Arizona soils had no identifiable effect on virus sorption and inactivation under both saturated and unsaturated conditions, which agrees with the results obtained by Gerba et al. (1981) and Moore et al. (1981).
Organic Matter Content
Contradictory results about the role of natural OM in the sorption of viruses onto soils have been reported. Gerba et al. (1981) found that sorption of Group I viruses, for which sorption was significantly associated with soil characteristics, was affected by the amount of OM for the soils studied, even though the OM content was quite low (ranging from 0.27 to 4.2%). Enhanced virus attachment to porous media with the presence of organic coating was observed and hydrophobic reactions were suggested as being responsible for the observed higher sorption of lipid-containing phage (Bales et al., 1991; Kinoshita et al., 1993). However, Burge and Enkiri (1978a) suggested that the high organic carbon content of a soil might have inhibited virus sorption by blocking or impeding the pathways to sorption sites. Sobsey et al. (1980) found that organic soil materials were comparatively poor sorbents for poliovirus. Moore et al. (1981) showed a strong negative correlation between poliovirus sorption and OM content, which was attributed to the low isoelectric point of soil OM that made it anionic at the pH values of natural systems. Other researchers also found that organic materials were poor adsorbers of viruses and made only small contributions to the removal of viruses (Funderburg et al., 1981; Fuhs and Taylor, 1982; Bitton et al., 1986). Soluble organics have been shown to compete with viruses for sorption sites on mineral surfaces, enhancing virus movement (Gerba et al., 1975; Bixby and O'Brien, 1979; Goyal and Gerba, 1979; Bitton et al., 1986; Pieper et al., 1997).
Compared with the other soils used in this study, the Georgia soil has a high OM content. The samples collected at the outflow were dark brown in color, indicating the presence of soluble OM in the outflow solution. The high outflow virus concentrations measured for the Georgia soil in both the saturated and unsaturated experiments indicated that the overall effect of OM as part of the soil composition and in the dissolved form was to lower the retention capacity of the soil for MS-2 and X174. The little difference for the outflow concentration of viruses between saturated and unsaturated experiments was not in agreement with the results reported by Sobsey et al. (1980). In that study, the organic soil materials proved to be poor sorbents for poliovirus under saturated conditions, but gave at least 95% virus removal under unsaturated conditions.
Film Straining
Film straining is considered important if the ratio of colloid size to the porous media's characteristic grain size exceeds 0.05 to 2 (Herzig et al., 1970; Tien and Payatakes, 1979). In our experiments this ratio is much smaller (approximately 0.001). Therefore, film straining should not be a significant factor influencing virus removal. We calculated the water film thickness in the unsaturated columns based on the equations proposed by Wan and Tokunaga (1997). The term d10, which is the grain size at 10% sieved mass and an effective grain diameter for description of hydraulic properties of soils, was used as the diameter of soil particles. The d10 values for different soils were calculated based on textural information listed in Tables 1 and 2. The calculated water film thickness was 19 nm for Delaware 1, 16 nm for Delaware 2, 21 nm for California, 15 nm for Arizona, and 16 nm for Georgia soils. These values are slightly less but still close to the diameters of the two viruses (26.3 nm for MS-2 and 23 nm for X174). The Arizona and Georgia soils have the thinnest water films among the five soils, but have the smallest extent of virus removal. This indicates that film straining was probably not a significant factor for increased virus removal in our unsaturated experiments.
Water Content Effect in Different Soils
Previous studies have shown that viruses are usually removed more extensively during unsaturated transport than during saturated transport (Lance and Gerba, 1984; Powelson et al., 1990; Powelson and Gerba, 1994; Poletika et al., 1995). However, our results in this study indicated that the extent of increased sorption or inactivation at low soil water content depends on properties of the soils. For example, the California and Arizona soils showed little difference between the saturated and unsaturated virus transport, but the two Delaware soils exhibited significantly greater virus retention and inactivation during unsaturated transport than during saturated transport. This suggests that the solid surface properties play an important role in influencing the extent of water content effect on virus behavior.
The increased virus removal under unsaturated flow conditions has been attributed to either increased inactivation or enhanced sorption. During unsaturated flow, viruses move through the soil in thinner films of water and will be drawn nearer to the soil particles than during saturated flow. This would increase the potential for virus sorption, thereby decreasing the virus penetration depth (Lance and Gerba, 1984). The air–water interface (AWI) may also contribute to increased sorption and inactivation of viruses (Trouwborst et al., 1974). Many researchers have attributed the increased removal of viruses and other colloid-sized particles under unsaturated flow conditions to sorption at the AWI (Powelson et al., 1990; Wan and Wilson, 1994; Wan et al., 1994; Powelson and Mills, 1996; Schäfer et al., 1998; Jewett et al., 1999). Thompson et al. (1998) and Thompson and Yates (1999) suggested that forces associated with the air–water–solid (where the solid is a hydrophobic surface) interface or triple-phase boundary (TPB), not the AWI alone, led to the inactivation of MS-2 in their studies. They hypothesized that as a virus particle adsorbs at the AWI, hydrophobic domains of the virus protein capsid partition out of the solution and into the more nonpolar gas phase, and such exposed domains are susceptible to forces at the TPB, which is influenced by the surface properties of the solid that are not present at the AWI. Results from this study strongly suggest that the increased sorption and inactivation at the solid–water interface (SWI) or reactions at the TPB rather than at the AWI alone are more important mechanisms for the enhanced sorption under unsaturated conditions. This conclusion is consistent with the results from the column study by Chu et al. (2001), which was specifically designed to differentiate the role of AWI and SWI in virus retention by using reactive and nonreactive sands. It is also conceivable that viruses sorbed on the surface of suspended clay particles and were flushed out of the columns, which diminished the AWI effect.
Comparison of the Behavior of X174 and MS-2
Under saturated flow conditions, the outflow concentrations of MS-2 were a little higher than those of X174 in the California and Arizona soils. However, this trend was reversed in the two Delaware soils, in which the outflow concentration of MS-2 was much lower than those of X174. The different isoelectric points of the viruses might be responsible for the observed lower removal of MS-2 than X174 in the California and Arizona soils. X174 has a higher isoelectric point (6.6) than MS-2 (3.9), so it possesses less net negative charge at the experimental pH of 7.5. Therefore, the repulsion between X174 particles and the negatively charged soil particles is less significant than the repulsion between MS-2 and soil particles. The difference in isoelectric points was also suggested as the reason for the greater removal of X174 than MS-2 in sand columns observed by Jin et al. (1997). However, the same effect of the isoelectric point on the behavior of MS-2 and X174 in the two Delaware soils was not observed. Instead, a greater amount of MS-2 was removed than X174. It is postulated that the reactivity of metal oxides and the low pH of Delaware soils overwhelmed the effect of electrostatic properties (i.e., the isoelectric point) in the two Delaware soils. It was also observed that MS-2 was much more reactive with the metal oxides than X174.
Under unsaturated flow conditions, the effects of water content further complicated the trend of differences exhibited by the two viruses. There was nearly no difference in transport and retention between X174 and MS-2 observed in the California and Arizona soils. In the Delaware soils, on the other hand, the difference between X174 and MS-2 was more pronounced in the unsaturated than in the saturated experiments, indicating that MS-2 was much more sensitive to the effect of water content in the presence of metal oxides.
Collision Efficiency
The collision efficiency factor (
), which describes the probability of colloids attaching after making contact to porous media grains, is an important parameter in filtration models. To calculate , the single collector efficiency (
), which is the probability of contact between transported colloids and filter grains, was calculated based on the following (Yao et al., 1971; Rajagopalan and Tien, 1976):
 | [1] |
D, I, and G are the colloid collector collision caused by Brownian motion, interception, and settling, respectively; As is the Hamaker constant; kB is the Boltzman constant (kg m2 s-2 K-1); T is the temperature (K); µ is the fluid viscosity (Pa s-1); dP is the diameter of viruses (m); dg is the diameter of the porous media grains (m) (set equal to d10 of each soil to relate to hydraulic properties of soils); v is the pore water velocity (m s-1); 
P is the virus density (Kg m-3); F is the fluid density (Kg m-3); and g is the gravitational constant (m s-2). The term As was calculated from the following:
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) was then calculated from the following equations (Tien, 1989):
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 | [5] |
(m-1) is the filtration coefficient and L is the column length (m). The C/C0 values from soils such as the Delaware soils were still increasing after initial breakthrough, suggesting that viruses attached to favorable sites first and the attachment efficiency decreased afterwards with time. The values are, therefore, not constant for these soils. The values at times of initial virus breakthrough for the Delaware soils are listed in Table 5. For the California, Arizona, and Georgia soils the C/C0 values at the plateau were used to calculate (Table 5). The Delaware soils and the California soil have higher values than the Arizona and Georgia soils. The values obtained from unsaturated columns are higher than those from saturated columns, except for the Georgia soil. One has to keep in mind that filtration theory in its present form is only applicable to saturated porous media. The values obtained under unsaturated conditions are actually "lumped" values, which include the effects of the air–water interface, film flow, and straining, etc. It is obvious that small changes of the water content may lead to significant changes of the values. Therefore, the calculated values under unsaturated conditions allow only a qualitative comparison between the experiments and should not be used for prediction.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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The increased virus removal during transport under unsaturated flow conditions through the Delaware soils indicates that water content effect was significant, possibly because metal oxides were present on the solid surface. On the other hand, virus retention by the California and Arizona soils (which are characterized by high P and Ca contents, along with high pH), and in the Georgia soil (which has high OM content), was not affected much by changes in water content for reasons that are unclear at this time. The high viral removal efficiency of the metal oxides suggests a possibility of using materials with high metal oxides content as hydrological barriers for microbial contamination.
This study demonstrates that the water content effect depends heavily on the surface properties of porous media, suggesting that increased sorption to the solid–water interface or inactivation at the triple-phase boundary contributed greatly to the enhanced virus removal. However, because of the multiple variables involved and their possible interactions among each other in a complex soil system, it is difficult to evaluate the water content effect alone and impossible to examine the mechanisms responsible for the observed effect.
Results from this study indicate that there is very high variability in virus retention and transport through different soils and aquifer materials, depending on their properties (metal oxides, OM, pH, etc.) and the degree of water saturation. Therefore, it will be very difficult or impossible to predict viral transport behavior in porous media based on our limited understanding of virus behavior in complex soil systems. This conclusion has significant implications on the USEPA's decision to consider only karst, fractured bedrock, and gravel settings as sensitive aquifers for viral contamination in the new Ground Water Rule. More studies are needed to further investigate the hydrogeologic formations affecting ground water vulnerability to viral contamination and the physical and chemical properties governing viral fate and transport in the subsurface (including the unsaturated zone and capillary fringe) to justify such a decision.
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ACKNOWLEDGMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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X174 on soil. J. Environ. Qual. 7:536–541.Related articles in JEQ:
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