Adsorption of rotavirus and bacteriophage MS2 using glass fiber coated with hematite nanoparticles

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Leonardo Gutierrez a, Xuan Li b, Jinwen Wang b, Gordon Nangmenyi b, James Economy b, Theresa B. Kuhlenschmidt c, Mark S. Kuhlenschmidt c, Thanh H. Nguyen a,* aDepartment of Civil and Environmental Engineering, The Center of Advanced Materials for the Purification of Water with Systems, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA bDepartment of Materials Science & Engineering, The Center of Advanced Materials for the Purification of Water with Systems, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA cDepartment of Pathology, University of Illinois at Urbana-Champaign, Urbana, IL 61802, USA a r t i c l e i n f o Article history: Received 4 May 2009 Received in revised form 17 August 2009 Accepted 19 August 2009 Available online 29 August 2009 Keywords: Rotavirus Inactivation Reversible electrostatic adsorption Competition Hematite nanoparticles a b s t r a c t Batch and flow-through experiments were conducted to investigate the removal and inactivation of rotavirus (RV) and bacteriophage MS2 using glass fiber coated with hematite nanoparticles. Batch tests showed a high removal of MS2 (2.49  1011 plaque forming unit/g) and RV (8.9  106 focal forming unit/g) at a low concentration of hematite nanoparticles in solution (0.043 g/L and 0.26 g/L, respectively). Virus adsorption was, however, decreased in the presence of bicarbonate ions and natural organic matter (NOM) in solution, suggesting a great affinity of iron oxide nanoparticles for these competitors. Adsorption on hematite nanoparticles by MS2 and RV was also tested with aquifer groundwater under saturated flow conditions to mimic environmental conditions with promising results (8  108 plaque forming unit/g and 3  104 focal forming unit/g, respectively). Desorption of up to 63% of infectious MS2 and only 2% of infectious RV from hematite nanoparticles were achieved when an eluant solution containing beef extract and glycine was used. Transmission electron microscopy (TEM) images showed evidence of electrostatic adsorption of apparently intact MS2 and structurally damaged RV particles to hematite nanoparticles. Results from this research suggest that a cartridge made of glass fiber coated with hematite nanoparticles could be used as a point-of-use device for virus removal for drinking water treatment. ª 2009 Elsevier Ltd. All rights reserved. 1. Introduction The presence of pathogenic enteric viruses in water poses a significant risk to human health. Their extremely small size (23–80 nm) enables enteric viruses to penetrate soil, contaminating aquifers, and travel long distances in groundwater (Abbaszadegan et al., 2003; Borchardt et al., 2007). Natural removal of viruses by iron oxide/hydroxide coating on aquifer materials has been studied (Abudalo et al., 2005; Atherton and Bell, 1983). Columns packed with zero-valent iron or sand coated with ferric hydroxides have been suggested as efficient means for virus removal (Lukasik et al., 1999; You et al., 2005). * Corresponding author. Tel.: þ1 217 244 5965; fax: þ1 217 333 6968. E-mail addresses: lgutier4@illinois.edu (L. Gutierrez), xuanli2@uiuc.edu (X. Li), jeconomy@illinois.edu (J. Economy), tkuhlens@illinois. edu (M.S. Kuhlenschmidt), kuhlensc@illinois.edu (M.S. Kuhlenschmidt), thn@illinois.edu (T.H. Nguyen). Available at www.sciencedirect.com journal homepage: www.elsevier.com/locate/watres 0043-1354/$ – see front matter ª 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.watres.2009.08.031 w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8 Significant improvement for virus removal has been shown by filters amended with carbon nanotubes or inorganic nanoparticles (Brady-Estevez et al., 2008; Wegmann et al., 2008a,b). Rotavirus (RV) is the most common enteric virus that causes severe diarrhea, vomiting and acute dehydration among children (Wyn-Jones and Sellwood, 2001). Approximately 600,000 children die worldwide every year because of intestinal complications due to RV infection (Parashar et al., 2006). Although efficient vaccines against RV have already been developed (Dennehy, 2008), their high cost makes them inaccessible for certain markets, such as Latin America, Asia and Africa. Nevertheless, it is in developing countries where RV has a higher probability of infecting the general population because of lack of access to sanitary water (Gutierrez et al., 2007). The objective of this study is to evaluate the use of glass fiber coated with hematite nanoparticles for virus removal under environmentally relevant conditions. This filter could potentially be used as a point-of-use device for water treatment without producing harmful disinfection by-products (DBPs) at developing nations at which water treatment facilities would be unavailable. In this study we used group A porcine rotavirus strain OSU and MS2 bacteriophage to investigate the ability of glass fiber coated with hematite nanoparticles for virus removal. Rotavirus is an icosahedral non-enveloped double stranded RNA virus measuring approximately 75 nm in diameter (Bridger et al., 1982). Bacteriophage MS2 (ATCC 15597B1) is a single-stranded RNA icosahedral bacteriophage measuring w26 nm in diameter (Van Duin, 1988). Many previous studies have used MS2 and other bacteriophages as model enteric viruses for water disinfection experiments. However, only a few have utilized RV on common disinfection technologies, such as chlorine and UV light (Espinosa et al., 2008; Nasser et al., 2006). Other studies have well reported electrostatic adsorption of MS2 to different materials (Wegmann et al., 2008a,b). However to the best of our knowledge, our study is the first to report rotavirus adsorption by electrostatic interactions. 2. Materials and methods 2.1. Preparation and characterization of glass fiber coated with hematite nanoparticles The hematite nanoparticles were synthesized and coated on the glass fiber at the same time. We, first, wrapped a glass rod with a glass fiber mat (Craneglas 230) with 7% polyvinyl alcohol (PVA) binder. This cartridge was dipped into a 0.5 M FeCl3 solution for 3 min and then heated at 90 C for 5 min. The cartridge was then immersed in a 15% NH4OH solution for 3 min, after which it was heated at 190 C for 4 h and finally washed and dried at 80 C. The final load of hematite nanoparticles in the glass fiber was w25% in mass. For batch experiments, the glass fiber coated with hematite nanoparticles was cut into w0.050 g pieces. For flow-through experiments the cartridge was packed in a column measuring 1.5 cm in diameter and 13.2 cm high. Brunauer-Emmett-Teller (BET) surface area and microand mesoporous volumes were carried out on an Autosorb-1 apparatus (Quantachrome) following the standard procedure (Rouquerol et al., 1999). All samples were degassed at 100 C until the outgas pressure rise was below 5 mmHg/min prior to analysis. Nitrogen isotherm obtained at 77 K in the appropriate relative pressure ranges was used for subsequent calculations. The BET equation was used to determine the surface area. The Dubinin-Radushkevich (DR) equation was used to deduce micropore volumes, i.e., total volume of pores with diameter <2 nm. The total pore volume was estimated from the amount of nitrogen adsorbed at P/Po ¼ 0.95. The mesopore volume (i.e., total volume of pores with diameter 2–50 nm) was calculated by subtracting the volume of micropores from the total pore volume at a relative pressure of 0.95. Wide angle X-ray diffraction (WAXD) experiments were carried out on a Rigaku D/Max-b diffractometer with a copper X-ray source controlled by MDI’s DataScan. Iron oxide nanoparticle powders were evenly distributed on a piece of doublesided tape on a glass slide. The parameters used were 45 kV and 20 mA, the scanning angle range (2q) was 15–80, and the scanning rate was 0.6/min, with a step increment of 0.05 2.2. MS2 preparation and plaque forming unit (PFU) assay MS2 phage was replicated and purified as described (Kitis et al., 2003) with the following modifications. Briefly, Escherichia coli (ATCC 15597) were grown in tryptic soy broth solution (TSB) and then inoculated with MS2. MS2 was purified by sequential centrifugation and microfiltration through 0.2-mm and 0.05-mm low-protein-binding polycarbonate track-etched membranes (Whatman Nucleopore, USA) to remove debris. Nutrients, microbial products and small debris were removed by using a 100-kDa membrane (Koch Membranes, USA) in a Millipore ultrafiltration unit (Whatman Nucleopore, USA), using a previously filtered and autoclaved 1 mM NaCl solution. The final MS2 stock was stored at 4 C at a concentration of w1011 PFU/mL. MS2 enumeration was performed following the double agar layer procedure (Adams, 1959). Briefly, the plaques, formed due to the inoculation of E. coli with MS2 at 37 C for 16 h, were counted. Only the plates that had from 20 to 300 plaques were used for calculation of MS2 concentration. 2.3. Rotavirus preparation and focus forming unit (FFU) assay Group A porcine rotavirus OSU strain was obtained from the American Type Culture Collection (catalog # VR892). Rotavirus was propagated in embryonic African green monkey kidney cells (MA-104 cells) and was extracted from culture as described (Rolsma et al., 1994). In lieu of gradient centrifugation, rotavirus was purified following the same protocol as MS2, except the nanofiltration step in which a 0.05-mm membrane was used. To prevent the dissociation of the outercapsid proteins (Ruiz et al., 1996), rotavirus was processed and stored in 1 mM NaCl plus 0.1 mM CaCl2 during the 100 kDa ultrafiltration. The final RV stock was stored at 4 C at a concentration of >106 FFU mL1. This purification procedure does not discriminate triple layer particles (TLP) from double layer particles (DLP). Rotavirus infectivity assays, or focus w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8 5199 forming unit tests (FFU), were carried out following the procedures described (Rolsma et al., 1998). 2.4. Solution chemistries Several chemically different solutions were prepared (Table 1) for testing MS2 and RV adsorption to hematite nanoparticles. The solutions were prepared immediately before use by utilizing Nanopure water of a resistivity of 18 MU cm (Millipore, Barnstead, USA) and high grade reagents, and then filtered using a 0.2-mm membrane. Artificial groundwater (AGW, Ionic strength w1.5 mM) was synthesized according to specific parameters for uncontaminated groundwater (Ryan et al., 1999). Newmark groundwater (NGW) was collected from a natural aquifer located beneath the Newmark Civil Engineering Laboratory (205 N. Matthews, Urbana, Illinois, 61801); its water has been characterized and used in previous studies (Li et al., 2003). Prior to use, NGW was greensand-filtered to remove manganese and iron and, then passed through a 0.2-mm membrane to separate out large, suspended particles. Content of dissolved organic carbon (DOC) was measured using a Phoenix 8000 TOC Analyzer (Dohrmann, USA). Final total organic carbon (TOC) concentration of NGW was 2.35 mg/L. Suwannee river natural organic matter (SRNOM) from the International Humic Substances Society (IHSS, St. Paul, MN) was used to simulate dissolved organic matter (DOM) in solution. The procedure for NOM solution preparation was previously described (Nguyen and Elimelech, 2007). NOM solution for fluorescence correlation spectroscopy (FCS) experiments was prepared in the dark to prevent photodegradation. The TOC concentration of the NOM solution, determined using a Phoenix 8000 TOC Analyzer (Dohrmann, USA), was 101.4 mg/L. The stock of SRNOM solution was stored in the dark at 4 C. 2.5. Measurement of electrophoretic mobility (EPM) for viruses and hematite nanoparticles Solutions in Table 1 were mixed with RV, MS2, or hematite nanoparticles to a final concentration of w104 FFU/mL, w1010 PFU/mL, and w0.74 mg/mL, respectively. These concentrations ensured an optimal signal for electrophoresis measurements. EPM was determined using a ZS90 Zetasizer instrument (Malvern, UK) and 1-mL clear disposable zeta cells (DTS1060C, Malvern). A minimum of 3 measurements was conducted for every solution condition. Several solutions in Table 1 included the addition of hematite nanoparticles with SRNOM to measure changes to EPM in the presence of negatively charged NOM. This set of measurements was converted to zeta potential with the Smoluchowski equation using Dispersion Technology Software (v5.10, Malvern 2008). To find the isoelectric point (IEP) of MS2, RV, and hematite nanoparticles, EPM was measured using a 1 mM NaCl solution. The range of pH tested fluctuated from 3 to 9 and was adjusted by adding high grade hydrochloric acid (0.1 M HCl) and sodium hydroxide (1 M NaOH). A minimum of 3 measurements was conducted for every pH selected. pH was determined using an Orion 3 Star pH meter (Thermo, USA). 2.6. Determination of hydrodynamic diameter of MS2 and rotavirus by dynamic light scattering (DLS) Hydrodynamic diameter of MS2 and RV was determined using a ZS90 Zetasizer instrument (Malvern, UK) for each solution tested in this study (Table 1). MS2 or RV was added to the solutions until a final concentration was reached of Table 1 – Chemical composition of solutions used in batch and flow-through experiments. Chemical Composition pH MS2 Rotavirus Hematite Size (nm) Zeta potential (mV) Energy Barrier (kT) Size (nm) Zeta potential (mV) Energy Barrier (kT) Zeta potential (mV) 1 mM NaCl 5.9 29 28 (3.9) 0 127 22.8 (0.3) 0 27.7 (2.2) 1 mM NaHCO3 8.2 30 31.9 (3.7) 15.2 128 23.5 (0.2) 46.6 26.9 (1.3) 0.5 mM NaHCO3 7.9 30 28.5 (1.0) 6.7 128 23.9 (1.4) 25.3 15.8 (0.9) 0.1 mM NaHCO3 7.6 30 26 (0.8) 0.6 127 22.1 (0.4) 2.4 4.3 (0.7) 1 mg/l TOC 5.9 30 28.2 (3.6) 127 22.5 (0.9) 25.9 (0.4) 1 mg/l TOC, 1 mM NaCl 5.9 29 24.7 (1.79) 15.9 128 22.5 (0.2) 56.4 38.9 (2.2) 1 mg/l TOC, 1 mM MgCl2 5.9 30 23.5 (3.8) 10.6 127 22.2 (0.6) 40.5 27.7 (2.3) 1 mg/l TOC, 1 mM CaCl2 5.9 31 13.7 (0.8) 3.2 127 11.8 (0.4) 2.5 17.9 (0.3) 1 mg/l TOC, 0.1 mM NaCl 5.9 30 28.8 (0.6) 19.8 127 22.2 (0.2) 54.5 37.9 (1.8) 1 mg/l TOC, 0.1 mM MgCl2 5.9 30 28.8 (1.2) 12.6 126 22.7 (1.1) 39.1 25.9 (1.0) 1 mg/l TOC, 0.1 mM CaCl2 5.9 29 19.5 (2.8) 6.4 125 16.9 (0.6) 21.7 21.7 (2.2) 0.1 mg/l TOC 5.9 31 25.4 (1.9) 128 22.3 (0.3) 26.2 (1.4) 0.1 mg/l TOC, 0.1 mM NaCl 5.9 30 24.9 (4.79) 16.3 128 22.9 (1.3) 59.0 34.7 (1.2) 0.1 mg/l TOC, 0.1 mM MgCl2 5.9 31 23.8 (5.0) 11.9 128 21.3 (0.4) 42.8 26.2 (1.4) 0.1 mg/l TOC, 0.1 mM CaCl2 5.9 30 18.6 (3.6) 7.1 128 16.9 (1.0) 25.9 20.8 (2.7) Newmark Groundwater: 307 mg/L as CaCO3 Hardness, 290 mg/L as CaCO3 Alkalinity, pH 7.3, 2.35 mg/L TOC 7.3 34 11.5 (0.5) 2.7 126 9.7 (0.9) 8.3 18.7 (1.1) Artificial Groundwater: 1 mM NaHCO3, 0.5 mM NaCl, 0.02 mM KCl, 1 mg TOC/L, pH 8.2. 8.2 29 23.6 (0.1) 15.6 128 22.2 (0.6) 57.9 46.2 (0.4) 5200 w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8 w1010 PFU/mL and w104 FFU/mL, respectively. These concentrations allowed us to use attenuation of 10 and a Polydispersity index (PDI) close to 0.2. Attenuation index denotes the percentage of laser light that enters the sample cuvette. For an index of 10, only 30% of the nominal laser power is used. Polydispersity index is a width parameter of the cumulant analysis of size. A minimum of 3 measurements per sample was recorded and a total of 3 samples per each virus was processed. 2.7. Determination of SRNOM diffusion coefficient using fluorescence correlation spectroscopy (FCS) FCS was used to determine the diffusion coefficient of SRNOM (Lead et al., 2000). Briefly, for a solution with 10 mg/L TOC at pH 6, an optimal average counting rate of w 4 KHz was generated. The final pH was measured as 6. Experiments were conducted at 20 C. The confocal FCS setup used one photon excitation at 488 nm. The power of the laser was 55 mW at 31.9%. A minimum of 5 FCS spectra per sample were recorded and a total of 6 samples were processed. Autocorrelation curves were fitted using one component model. 2.8. Transmission electron microscopy (TEM) MS2 and RV samples with hematite nanoparticles were investigated using TEM technique by conventional negative staining. Pellets of RV solution were obtained by centrifugation at 24,000 rpm (48,608  g) for one hour. To preserve RV structural details, a few drops of Karnovsky’s fixative were added to the top of the pellet and allowed to set for 20 min. Viruses and hematite suspensions were applied to holeycarbon–coated, 300-mesh, copper grids. Tungsten acetate and uranyl acetate were used as stains for MS2 and RV, respectively. All the samples were examined using a Cryo TEM (JEM- 2100, JEOL, Tokyo, Japan) at 200 kV accelerated voltage. 2.9. Batch experiments Batch tests were prepared using 300-mL Pyrex bottles for MS2 and 50-mL Pyrex bottles for RV. These glass containers were cleaned using detergent and DI water and thereafter rinsed with Nanopure water, dried in an oven, and autoclaved. The bottles were filled with viral solution and varied mass of glass fiber coated with hematite nanoparticles. Air bubbles were avoided by filling the container to the top with viral solution and then covering it with Parafilm. The initial concentration of the solution was w107 PFU/mL for MS2 and w104 FFU/mL for RV. The bottles were shaken at 200 rpm in a horizontal shaker and samples were taken every 30 min for 3 h for MS2 and every 15 min for 90 min for RV. 1 mL or 0.25 mL of solution were removed for kinetics experiments with MS2 or RV, respectively. The same volume of buffer solution was added back to the bottles after removing solution. Control experiments, performed for MS2 and RV using glass fiber substrate with no coat of hematite nanoparticles, showed no removal of viruses at 22 C during the 3 h of testing for MS2 and 90 min for RV. First-order kinetic rate constants (k) for virus removal were estimated by fitting the virus concentrations measured throughout the experiment. Reversibility of virus adsorption was studied by eluting with beef extract and glycine as previously reported (You et al., 2003). Batch reactors were prepared following the protocol described in this section. However only for these experiments hematite nanoparticles without the glass fiber, as colloidal nanodispersed particles, were added to the solution containing either w107 PFU/mL or w104 FFU/mL. After the adsorption period, beef extract and glycine were added directly to the batch reactor at concentrations ranging from 1.5% to 3% [wt/vol] and 50 mM to 100 mM, respectively, while raising the pH to 8 and 9. In addition, colloidal hematite nanoparticle samples after adsorption and desorption of viruses were taken for TEM analysis. 2.10. Flow-through experiments Flow-through experiments were conducted to test the adsorption capacity of glass fiber coated with hematite nanoparticles under saturated flow conditions and selected solution chemistries. We refer to the experiments in which virus containing solution was pumped continuously through the cartridge as flow-through experiments. For every test, 1000 mL of w107 PFU/mL MS2 and 200 mL of w5  104 FFU/mL suspensions were used. The viral solution was pumped using a peristaltic pump at a flow rate of w3 mL/min through the flow-through to ensure a saturated flow at 22 C. Samples from the outflow were collected every 5 min (15 mL). Blank tests were also conducted to measure possible adsorption of viruses to tubing or glass fiber with negative results. Finally, after the virus inflow was ceased, a 1.5% beef extract and 50 mM glycine solution at a pH of 8 or 9 was used to elute the viruses previously adsorbed by the hematite nanoparticles for testing viability. 3. Results and discussion 3.1. Characterization of hematite nanoparticles According to X-ray diffraction analysis, the particles are hematite with no other phases present. The particles are spherical with diameters ranging from w3 to 20 nm. The BET surface area of the iron oxide nanoparticles was measured as 80.75 m2 g1, whereas the total pore volume (P/P0 ¼ 0.95) was measured as 8.35  102 cm3 g1. The fraction of micropore volume is 34.1% (2.85  102 cm3 g1), while the mesopore volume is 65.9% (5.50  102 cm3 g1). The iron oxide nanoparticles coating the glass fiber have small particle size, high surface area, and more hydroxyl groups (Hsin-Yu et al., 2005) than granular particles. The BET surface area of iron oxide-coated sand is only about 3–4 m2/g, which limits the system efficiency and the emptybed contact time. The fiber form substrate provides the larger surface area needed to significantly enhance the virus adsorption kinetic and capacity, and enables the assembly filter to have much lower pressure drop compared to other forms of substrates (Yue et al., 2001). Transmission electron micrograph revealed a mean diameter of 10.78 (0.72) nm and the presence of nanoparticle aggregates ranging on average from 100 to 300 nm in size. No w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8 5201 monodispersion of nanoparticles was observed. SEM images showed a coating of hematite nanoparticles on the glass fiber substrate. The glass fiber had a rod shape with an approximated diameter of 7 mm. The hematite nanoparticles covered the majority of the glass fiber’s exposed surface as a heterogeneous layer in thickness. 3.2. Size of viruses Mean hydrodynamic diameters of MS2 and RV in all the solutions listed in Table 1 were measured as 30.83 (0.31) nm and 127.15 (1.05) nm, respectively. Low polydispersity index of 0.15 for MS2 and 0.21 for RV suggested monodispersed population of MS2 and RV for every solution condition in Table 1. TEM images revealed mean MS2 and RV diameters of 25.42 (0.93) nm and 74.57 (1.32) nm, respectively, which are in accordance with previously reported data (Bridger et al., 1982; Van Duin, 1988). The difference in diameter between DLS and TEM (w21% for MS2 and w70% for RV) denotes the variation between hydrodynamic diameter (hydrated particles) and dry virus diameter. 3.3. Diffusion coefficient of SRNOM, MS2 and RV The fitting of the autocorrelation curve was directly deduced with one component model, and indicated only one fairly pure, homogeneous population present in solution. Diffusion coefficient (D) of SRNOM was averaged as 106.52 (3.32) mm2 s1, which was assumed to be for a single macromolecule in solution. This value is comparable to previously reported diffusivities for SRNOM fractions (Lead et al., 2000). Because of their nearly-spherical icosahedral shape, the Stokes-Einstein relation was used to convert the hydrodynamic diameters of MS2 and RV to diffusion coefficients. Diffusivities for MS2 and RV were calculated as 13.89 and 3.37 mm2 s1, respectively. 3.4. Zeta potential of viruses Isoelectric points of MS2, RV, and hematite nanoparticles were determined as 3.6, 4.5, and 6.9, respectively (Fig. 1). Although to the best of our knowledge the isoelectric point of RV has not been measured before, the values for MS2 are consistent with previous studies (Yuan et al., 2008). Indeed, under the environmental range of pH selected for this research (6–9), MS2 and RV showed a highly negative potential, while hematite nanoparticles were positively charged until reaching their isoelectric point (0 mV at pH 6.9). In addition, EPM were determined for MS2, hematite nanoparticles, and RV under every solution condition listed in Table 1. These values were converted to zeta potential using Smoluchowski’s equation. The total interaction energy between MS2 or RV and the hematite plate surface was calculated as the sum of repulsive electrostatic and retarded van der Waals interactions (Gregory, 1981; Hogg et al., 1966). A Hamaker constant (A) of 4  1021 J was used (Penrod et al., 1996). The only condition at which MS2 and hematite nanoparticles showed no energy barrier at all was at 1 mM NaCl, an effect caused by the isoelectric points of MS2 and hematite nanoparticles. While MS2 showed a negative potential, hematite nanoparticles were positively charged. However, when bicarbonate was present in solution for concentrations ranging from 0.1 to 1 mM (pH 7.6– 8.2), MS2 showed energy barriers from 0.56 to 15.2 kT, respectively. These energy barriers were produced because of the negative potential exhibited by both MS2 and hematite nanoparticles. For the rest of the conditions at which NOM was present in solution, hematite showed a negative potential. Considering the low pH (5.9) of these solutions, hematite should have been positively charged. However, when charged NOM attached to the positively charged hematite nanoparticles, their potential became negative. This effect, if combined with the similar negative charge exhibited by MS2, would create energy barriers that would prevent successful collisions. Nonetheless, when divalent cations were added to the NOM solution (Mg2þ and Ca2þ), the potential of MS2 and hematite nanoparticles became less negative. Ca2þ in particular had a more pronounced effect in comparison to Mg2þ, which might help explain the less negative potential of hematite in NGW, although it had a high NOM content (energy barrier of 2.7 kT). Similar to MS2 experiments, RV and hematite nanoparticles showed no energy barrier for the 1 mM NaCl condition because of their isoelectric points. However, they were present at 0.1–1 mM NaHCO3 in solution, although their magnitudes (2.38–46.6 kT, respectively), were higher than those of MS2. Although RV has a higher isoelectric point than MS2, its larger size produces higher energy barriers. Negatively charged hematite nanoparticles in the presence of NOM produced energy barriers at every condition. Nevertheless, the magnitude of these energy barriers was considerably higher in comparison to MS2. 3.5. Batch test results for MS2 and rotavirus 3.5.1. Adsorption of MS2 and rotavirus to hematite nanoparticles under non-competing conditions in solution We first measured viral adsorption on hematite nanoparticles in solution containing 1 mM NaCl as the basis for quantitative comparison of the effect of other ions and NOM on adsorption. Adsorption capacity is defined as the number of infectious virus particles (FFU or PFU) adsorbed per gram 2 4 6 8 10 -3 -2 -1 3 2 1 0 (MPE µ sm 1- mcV/ 1- ) pH Rotavirus MS2 Hematite Fig. 1 – Zeta potential measurement for MS2, RV and hematite nanoparticles. 1 mM NaCl solution was used as background solution. 5202 w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8 of hematite nanoparticles in solution. The adsorption capacity for MS2 in a 1 mM NaCl solution for 2 log removal was 2.33  1011 PFU/g for pH 6 and 2.49  1011 PFU/g for pH 8. The adsorption followed a pseudo-first-order reaction with kinetic rate constants (k) of 0.030 min1 and 0.036 min1, respectively (Fig. 2a). For a 1.5 log removal of RV, the adsorption capacity was 2.6  106 FFU/g and the rate constant was 0.040 min1 (Fig. 2b). When the concentration of hematite nanoparticles in solution for the RV experiment was increased to 1.95 g/l, the kinetics rate constant increased to 0.357 min1 with a total removal of viruses (5 logs) and an adsorption capacity of 8.9  106 FFU/g from solution within the first 45 min. Another batch test under the same conditions was conducted, and the solution pH (starting at pH 9.0) was monitored and continuously adjusted every 30 min to pH 9 using 1 M NaOH. The solution experienced a high drop of four pH units during the first 30 min, showing that hematite acidifies the solution. Although under these conditions the adsorption capacity still remained high for MS2 (1.79  1011 PFU/g), the kinetic rate decreased to 0.016 min1. These results suggest an almost negligible influence of proton concentration at a pH range from 6 to 9 on the adsorption of MS2 with no competing ions in solution. Using classic DLVO calculations, for a 1 mM NaCl solution at pHs 6 and 7, we found no energy barrier and one of 0.9 kT, respectively. Adsorption of MS2 to hematite nanoparticles at pH values below 7 is electrostatically favorable. Above pH 7 the hematite nanoparticles acquired a negative charge, producing a small energy barrier (up to 16.1 kT at pH 9). However, adsorption of MS2 to hematite nanoparticles at pH 6 and 9 were similar. These outcomes indicated that both viruses adsorbed to hematite nanoparticles, confirming the adsorption property of iron oxides already described in the literature (Ryan et al., 2002). Due to their relatively high surface area and IEP, hematite nanoparticles have shown fast kinetic rates and a high adsorption capacity for MS2 and RV under noncompeting conditions. Nevertheless, in natural water systems many competitors for adsorption sites are found. 3.5.2. Effect of bicarbonate ions on adsorption of MS2 and RV to hematite nanoparticles When the background ion solution was 1 or 0.1 mM bicarbonate (pH 8.2 and 7.6, respectively), no removal of MS2 or RV was observed and the pH of the solution remained stable until the end of the experiment. However, when the concentration of hematite nanoparticles in solution was increased 3.5 times to 0.150 g/L in a 0.1 mM NaHCO3 solution, removal of MS2 was detected with the adsorption capacity decreased one order of magnitude to 1.7  1010 PFU/g and the kinetic rate constant to 0.016 min1. This decrease of pH from 7.5 to 4.6 suggests that the carbonate species were almost completely adsorbed by the hematite. Therefore, the removal of viruses decreased because many adsorption sites were occupied by the adsorbed bicarbonate ions. When the bicarbonate concentration was kept at 1 mM, but the concentration of hematite in solution was increased to 0.107, 0.215, and 0.32 g/L, no removal was detected. MS2 and RV removal was detected when the concentration of hematite nanoparticles increased to 0.43 g/L and 0.650 g/L, respectively. For MS2 removal, by 0.43 g/L, the adsorption capacity decreased to 2.7  1010 PFU/g (Fig. 2a). For RV removal, by 2.0 g/L hematite nanoparticles, the adsorption capacity was reduced to 8.3  105 FFU/g and all adsorption sites were depleted, reaching only a 0.64 log removal of RV. When the concentration of hematite increased to 3.9 g/L, 5 log removal of RV was observed after 90 min at a kinetic rate constant of 0.122 min1 and an adsorption capacity of 7.5  105 FFU/g (Fig. 2b). Our results suggest a great affinity of hematite nanoparticles for even low bicarbonate ions concentrations, implying that the attachment sites were reached more efficiently by bicarbonate ions than by viruses. Therefore, the adsorption capacity of hematite nanoparticles was consequently decreased by slightly more than one order of magnitude. A noticeable drop in pH of the solution was 0 30 60 90 -6 -4 -2 0 Log Rotavirus Removed Time (minutes) 1 mM NaCl - 0.26 g/L hematite 1 mM NaCl - 1.95 g/L hematite 1 mM bicarbonate - 2.0 g/L hematite 1 mM bicarbonate - 3.9 g/L hematite 1 mg/l TOC - 1.3 g/L hematite 1 mg/l TOC - 3.9 g/L hematite b 0 60 120 180 -8 -6 -4 -2 0 Log MS2 Removed Time (minutes) 1mM NaCl pH 6 0.043 g/L hematite 1 mM NaCl pH 8 0.043 g/L hematite 1mM bicarbonate - 0.32 g/L hematite 1mM bicarbonate - 0.43 g/L hematite 1 mg/l TOC - 0.65 g/L hematite a Fig. 2 – a) MS2 removal kinetics and adsorption onto hematite nanoparticles in 1 mM NaCl at pH 6 and 8; or 1 mM bicarbonate; or 1 mg/L TOC. b) Rotavirus removal kinetics and adsorption onto hematite nanoparticles in 1 mM NaCl; or 1 mM bicarbonate; or 1 mg/L TOC. w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8 5203 perceived every time adsorption of viruses was detected, suggesting that the bicarbonate ions had been exhausted due to their adsorption onto hematite nanoparticles. Hematite nanoparticles have relatively higher surface area, allowing more available sites for adsorption in comparison to granular media. According to our results, 0.32 g/L of hematite nanoparticles reduced the pH of a 1 mM NaHCO3 solution from 8.2 to 7.6, which corresponds to a decrease in [HCO3 ] of 0.9 mM. This ratio is of particular importance for calculating the performance of hematite nanoparticles in real systems. Hematite nanoparticles would be suitable for treated water already equilibrated with the atmosphere and close to neutral pH. The low bicarbonate concentration of these water systems (w0.01 mM) would only require w3.5 mg/L hematite for adsorbing this species. Any excess concentration of hematite nanoparticles would provide adsorption sites for viruses or other charged species in solution. 3.5.3. Competition by NOM with MS2 and RV for adsorption onto hematite nanoparticles To test for competition from NOM, a 1 mg/L TOC solution was prepared and tested under the different concentrations of hematite until virus removal was detected. No MS2 or RV removal was perceived when the hematite concentration was increased up to 0.43 g/L or 1.3 g/L, respectively. However, when the hematite concentration was further increased to 0.65 g/L, MS2 removal was detected at a kinetic rate and adsorption capacity of 0.008 min1 and 1.4  1010 PFU/g, respectively (Fig. 2a). For RV, the hematite concentration was increased to 3.9 g/L to obtain an adsorption capacity of 1.2  105 FFU/g and a rate constant of 0.032 min1. This result was one order of magnitude below non-competing conditions and close to bicarbonate batch test values (Fig. 2b). A second experiment was conducted in which the concentration of TOC was decreased to 0.1 mg/L and the concentration of hematite nanoparticles was fixed at 0.043 g/L for MS2 and 0.260 g/L for RV. No removal of viruses was detected at this low concentration of NOM. Note that zeta potential values for MS2 and RV in the presence of 0.1 or 1 mg/L TOC were almost the same as in the absence of it (1 mM NaCl), suggesting a negligible influence of NOM on the charge of viruses under these concentration conditions. Under the range of concentrations tested in this set of experiments, NOM proved to be an efficient competitor against MS2 and RV for available binding sites. The diffusivity of SRNOM measured in this study (106.52  3.32 mm2 s1) was higher than the diffusivity for MS2 and RV (13.89 and 3.37 mm2 s1, respectively). This high value of SRNOM diffusivity could allow NOM to outcompete viruses for adsorption sites. As a result, the addition of NOM provoked a dramatic drop of slightly more than one order of magnitude in the adsorption capacity of hematite for both viruses. Nevertheless, the addition of more mass of iron oxide was necessary to compensate for the competition effect for attachment sites for both MS2 and RV. However, hematite nanoparticles have the advantage of offering a more specific surface and, consequently, more available adsorption sites per gram than hematite as granular media. In comparison to bicarbonate conditions, NOM solutions did not experience change of pH at the end of the experiment, but of charge of hematite nanoparticles. According to our results, 1 mg/L TOC would be sufficient to cover the adsorption sites of 0.43 g/L hematite nanoparticles and not allow adsorption of MS2 (Fig. 2a). Although this ratio might be high, the NOM adsorbed to hematite nanoparticles is the charged fraction of the total population of NOM. In drinking water treatment, most of the charged organic matter is coagulated and flocculated in the first treatment steps, while uncharged species is absorbed to activated carbon. Hematite nanoparticles would be a feasible option for a portable device for virus removal for pretreated water. 3.5.4. Adsorption of MS2 and RV in the presence of aquifer and artificial groundwater Once competition between bicarbonate ions and organic carbon and MS2 and RV was confirmed, batch tests using artificial groundwater (AGW) and aquifer groundwater (NGW) were conducted. Different concentrations of hematite nanoparticles were utilized (0.043, 0.107, 0.430 and 0.645 g/L) until removal of MS2 was clearly detected at 0.9 g/L (Fig. 3a) with an adsorption capacity for MS2 of 6.9  109 PFU/g and a rate constant of 0.023 min1. This reduction represents a dramatic drop of 2 log units in comparison with non-competing conditions. The aquifer groundwater NGW contains a TOC composition higher than AGW (Table 1) and other ion content. NGW’s pH, close to one order of magnitude lower with respect 0 60 120 180 -4 -3 -2 -1 0 AGW NGW Log MS2 Removed Time (minutes) 0 30 60 90 Time (minutes) a -2 -1 0 0.3 g/L hematite 1.3 g/L hematite 2.0 g/L hematite Log Rotavirus Removed b Fig. 3 – Adsorption of MS2 (a) and RV (b) to hematite nanoparticles in the presence of AGW or NGW as background solutions. For MS2, a concentration of 0.9 g/L hematite was used for both experiments. For RV, 0.3 g/L, 1.3 g/L or 2.0 g/L hematite nanoparticles was used. 5204 w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8 to AGW, would reflect a lower concentration of HCO3 . Following a similar procedure as in AGW, the mass of hematite was sequentially increased from 0.043, 0.107, 0.430, and 0.645 to 0.9 g/L until a clear removal of MS2 was detected (Fig. 3a). Hematite’s adsorption capacity for MS2 was again reduced to 1.8  109 PFU/g with a kinetic rate of 0.016 min1. These last results indicate a higher content of competitors in NGW for MS2. Aquifer groundwater (NGW) was also used as a background for RV. When 2.0 g/L of hematite nanoparticles were added, the adsorption sites were depleted after 30 min and, as expected, the adsorption capacity was decreased close to 2 orders of magnitude (5.4  104 FFU/g) in comparison to noncompeting conditions (Fig. 3b). A 0.66 log removal was achieved under this condition. When the concentration of hematite was increased to 3.2 g/L and 3.9 g/L, the adsorption capacity increased to 1.5  105 and 2.1  105 FFU/g with 1 log and 1.83 log removed, respectively. For both viruses, the adsorption capacity of hematite nanoparticles experienced a drop of slightly 2 orders of magnitude in groundwater, reflecting the possible presence of more competitors in solution for binding sites than the previous conditions tested. This might explain why it was necessary to use a high concentration of at least 0.650 g/L hematite nanoparticles in order to adsorb organic matter and different charged species before small viruses like MS2 would be adsorbed. 3.5.5. Role of divalent cations in the adsorption of viruses to hematite nanoparticles Divalent cations have been shown to enhance adsorption of MS2 to silica surface coated with NOM (Pham et al., 2009). We conducted batch experiments to test whether divalent cations allow improved performance of the studied glass fibers coated with hematite nanoparticles. For both MS2 and RV, no enhanced adsorption was detected (Figs. 4 and 5). 3.5.6. Desorption of MS2 and RV The previous experiments establish that MS2 and RV are adsorbed (or inactivated) by hematite nanoparticles. In this next group of experiments it was found that MS2 activity could be reversibly dissociated by beef extract and glycine. MS2 recoveries were not highly dependent on beef extract, glycine concentration, or pH level and ranged between 18.18% and 63.41%. These results indicate that a considerable fraction of MS2 was still infectious during the attachment and detachment process and, therefore, reversibly adsorbed to the hematite nanoparticles. In addition, TEM micrographs of samples taken after the adsorption period reveal apparently intact MS2 adsorbed to the surface of hematite nanoparticle aggregates (Fig. 6a). These results suggest that MS2 adsorption -3 -2 -1 0 0.1 mM CaCl 2 0.1 mM MgCl2 1 mM NaCl Log MS2 Removed Log MS2 Removed Log MS2 Removed Time (minutes) a -3 -2 -1 0 1 mM CaCl 2 1 mM MgCl2 1 mM NaCl b 0 60 120 180 Time (minutes) 0 60 120 180 Time (minutes) 0 60 120 180 -3 -2 -1 0 0.1 mM CaCl 2 0.1 mM MgCl 2 0.1 mM NaCl c Fig. 4 – Influence of Ca2D or Mg2D and NOM on the adsorption of MS2 to hematite nanoparticles. a) 0.1 mM Ca2D, 0.1 mM Mg2D, 1 mM NaCl, 1 mg/L TOC, 0.645 g/L hematite nanoparticles. b) 1 mM Ca2D, 1 mM Mg2D, 1 mM NaCl, 1 mg/L TOC, 0.645 g/L hematite nanoparticles. c) 0.1 mM Ca2D, 0.1 mM Mg2D, 0.1 mM NaCl, 0.1 mg/L TOC, 0.107 g/L hematite nanoparticles. 0 30 60 90 -2 -1 0 1mM NaCl 1mM CaCl 2 1mM MgCl2 Log Rotavirus Removed Time (minutes) Fig. 5 – Influence of Ca2D or Mg2D and NOM on the adsorption of RV to hematite nanoparticles. The conditions are 1 mM Ca2D, 1 mM Mg2D, 1 mM NaCl, 1 mg/L TOC, and 3.9 g/L hematite. w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8 5205 to hematite nanoparticles did not lead to inactivation of a significant portion of MS2. Previous research (Ryan et al., 2002), however, suggests that the electrostatic forces of attraction of iron oxides are so strong, they cause viruses to disintegrate. In contrast to MS2 results, RV recoveries ranged from 0.5% to 2.1% and showed no dependence on beef extract, glycine concentration, or pH level. These results suggest that RV irreversibly adsorbed or became inactivated during the attachment process to hematite nanoparticles. Consequently, their outermost proteins, responsible for virulence, could have been affected by the electrostatic forces of attraction or disintegration of the viral particles. TEM micrographs showed RV with structural damage when hematite nanoparticles were present in solution (Fig. 6b). No RV visibly adsorbed to the surface of the hematite aggregates, suggesting that after the electrostatic forces compromised the integrity of RV, the viral particles broke apart and were released into solution. The observations that MS2 and RV exhibited different behavior to the electrostatic forces of hematite nanoparticles suggest that the inactivation of a given viral particle might depend on the proteins of its capsids or the robustness of its structure. 3.6. Flow-through test results for MS2 and rotavirus 3.6.1. Adsorption of MS2 and rotavirus to hematite nanoparticles under non-competing conditions in solution For a 1 mM NaCl solution, adjusted to pH 8, that contains a cartridge of 0.060 g hematite nanoparticles, breakthrough was observed for a minimum of 4 log removal for MS2. The adsorption capacity for this condition was 1.7  1011 PFU/g. When pH was kept at 6, the adsorption capacity dropped to 4.6  1010 PFU/g. These values were similarto batch conditions at the same pH. A similar set of experiments was conducted for RV. For a cartridge containing 0.060 mg hematite Fig. 6 – a) TEM image shows MS2 phages adsorbed to the surface of an aggregate of hematite nanoparticles. There is no noticeable decrease in the diameter of the viral particles and their integrity did not appear to be compromised. b) TEM image shows RV particles with compromised structure after coming into contact with hematite nanoparticles in solution. 0 10 20 30 40 50 -6 -4 -2 0 AGW NGW Log Rotavirus Removed Log MS2 Removed Bed Volumes 0 5 10 15 20 25 30 -4 -2 0 NGW AGW Bed Volumes a b Fig. 7 – Adsorption of a) MS2 and b) rotavirus on hematite nanoparticles in artificial and aquifer groundwater. In both cases, artificial groundwater presented fewer competitors than Newmark groundwater for virus adsorption on available adsorption sites. 5206 w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8 nanoparticles, no breakthrough was observed after 45 bed volumes. The adsorption capacity of 5  107 PFU/g for flowthrough conditions is one order of magnitude higher than a batch test at the same conditions, suggesting that flowthrough is more efficient in removing RV. 3.6.2. Adsorption of MS2 and RV in the presence of aquifer and artificial groundwater The mass of hematite nanoparticles in the cartridge for both experiments with AGW and NGW was 0.520 g. The adsorption capacity achieved until breakthrough was 1.1  109 PFU/mL and 8  108 PFU/mL for AGW and NGW, respectively (Fig. 7a). These results are roughly more than 2 orders of magnitude below the adsorption capacity of hematite under noncompeting conditions. The high concentration of NOM and other ions present in NGW or the bicarbonate and NOM content of AGW are responsible for the reduced adsorption of MS2. When similar cartridges were tested for RV removal, the adsorption capacity until 4 log removal for RV reached 3  104 FFU/g for NGW and 9  104 FFU/g for AGW (Fig. 7b). These results suggest that this cartridge can be used as a point-ofuse device to remove viruses from water with similar characteristics to groundwater. 3.6.3. Desorption of MS2 and RV Detachment of infectious MS2 and RV were also investigated using the same reagents and conditions as in batch tests. Initially, a 2.0  106 PFU/mL solution was injected to a column containing 0.130 g of hematite nanoparticles. The flow of viral solution was stopped when 1  109 PFU were injected into the column (500 mL) and, consequently, no PFU were detected inthe effluent. The viral solution was switched to a beef extract–glycene solution and samples of the effluent were taken. High recoveries ranging from 44.02% to 45.81% of infectious viruses were achieved (Fig. 8a), suggesting that a considerable fraction of MS2 were able to remain infective during the adsorption/ desorption process. These results are in agreement with batch experiments. However, the desorption process of RV did not release a high fraction of infectious viral particles as with MS2. The highest recovery was in the order of 1.53% of infectious RV (Fig. 8b). This result is also in accordance to batch tests. 4. Conclusion  Hematite nanoparticles showed high affinity for bicarbonate ions and NOM in solution. Adsorption capacity of hematite nanoparticles was reduced down to 2 log units when NOM and bicarbonate ions were present in solution in comparison to non-competing conditions.  Because hematite nanoparticles have high surface area, these particles allow virus adsorption even in the presence of bicarbonate and NOM in natural water.  Only a small fraction of infectious RV was successfully eluted in comparison to MS2, possibly due to structural damage to the capsid of RV when interacting with hematite.  FeCl3.6H2O and NH4OH are cost-effective and common chemical reagents, which may further promote manufacturability and commercialization for this innovation. In addition, our synthesis approach is facile and the calcination temperature ofironoxide nanoparticlesis relatively low. Based onthe price from Sigma-Aldrich, we calculated the material cost for one iron oxide-coated glass fiber filter. 1.69 g of FeCl3$6H2O and 2.2 mL of NH4OH (28–30% NH3) are required to generate 500 mg of hematite nanoparticles. Typical filter parameters include 7.5 g of glass fiber and 0.5 g of hematite nanoparticles. The total cost for a single cartridge was $0.18, which includes $0.00025 for glass fiber, $0.133 for FeCl3$6H2O and $0.050 for NH4OH. These cartridges can be used as point-of-use devices for virus removal for drinking water. Acknowledgements This work was partially supported by The WaterCAMPWS, a Science and Technology Center of Advanced Materials for the Purification of Water with Systems under the National Science Foundation agreement number CTS-0120978, USDA grant no. 2008-35102-19143, and the Fulbright Fellowship for LG. Hematite nanoparticles were synthesized and characterized by XL, 0 60 120 180 240 -6 -4 -2 2 0 MS2 in 1 mM NaCl Elution with beef extract and glycine Log ([MS2]/[MS2]0 Time (minutes) 0 30 60 90 120 -6 -4 -2 2 0 RV in 1 mM NaCl Elution with beef extract and glycine Log ([RV]/[RV] o) Time (minutes) a b Fig. 8 – Recovery of infectious MS2 using a solution of 1.5% beef extract in 50 mM glycine at pH 8 (a) and infectious rotavirus (b) using 3% beef extract in 100 mM glycine at pH 8. [MS2]/[MS2]0 is the ratio of MS2 concentration in the effluent over the initial MS2 concentration. [RV]/[RV]0 is the ratio of rotavirus concentration in the effluent over the initial rotavirus concentration. w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8 5207 JW, and GN under the direction of JE and the assistance of Amanda L. Hodges. Rotavirus cultivation was conducted by LG under the direction of TK and MK. MS2 and rotavirus TEM micrographs were carried out in the Frederick Seitz Materials Research Laboratory Central Facilities, University of Illinois, whichare partially supportedby the U.S. Department of Energy under grants DE-FG02-07ER46453 and DE-FG02-07ER46471. Other experiments, data interpretation and manuscript preparation were conducted by LG with THN’s supervision. r e f e r e n c e s Abbaszadegan, M., Lechevallier, M., Gerba, C., 2003. Occurrence of viruses in US groundwaters. Journal of the American Water Works Association 95 (9), 107–120. Abudalo, R., Bogatsu, Y., Ryan, J., Harvey, R., Metge, D., Elimelech, M., 2005. Effect of ferric oxyhydroxide grain coatings on the transport of bacteriophage PRD1 and Cryptosporidium parvum oocysts in saturated porous media. Environmental Science and Technology 39, 6412–6419. Adams,M.,1959.Bacteriophages.IntersciencePublishers,NewYork. Atherton, J., Bell, S., 1983. Adsorption of viruses on magnetic particles – I: adsorption of MS2 bacteriophage and the effect of cations, clay and polyelectrolyte. Water Research 17 (8), 943–948. Borchardt, M., Bradbury, K., Gotkowitz, M., Cherry, J., Parker, B., 2007. Human enteric viruses in groundwater from a confined bedrock aquifer. Environmental Science and Technology 41, 6606–6612. Brady-Estevez, A.S., Kang, S., Elimelech, M., 2008. A single-walledcarbon-nanotube filter for removal of viral and bacterial pathogens. Small 4 (4), 481–484. Bridger, J., Clarke, I., MsCrae, M., 1982. Characterization of an antigenically distinct porcine rotavirus. Infection and Immunity 35 (3), 1058–1062. Dennehy, P.H., 2008. Rotavirus vaccines: an overview. Clinical Microbiology Reviews 21 (1), 198–208. Espinosa, A.C., Mazari-Hiriart, M., Espinosa, R., Maruri-Avidal, L., Mendez, E., Arias, C.F., 2008. Infectivity and genome persistence of rotavirus and astrovirus in groundwater and surface water. Water Research 42 (10–11), 2618–2628. Gregory, J., 1981. Approximate expressions for retarded van der Walls interaction. Journal of Colloid and Interface Science 83 (1), 138–145. Gutierrez, M., Alvarado, M., Martinez, E., Ajami, N., 2007. Presence of viral proteins in drinkable waterdsufficient condition to consider water a vector of viral transmission? Water Research 41, 373–378. Hogg, R., Healy, T., Fuersten, D., 1966. Mutual coagulation of colloidal dispersions. Transactions of the Faraday Society 62, 1638–1651. Hsin-Yu, L., Yu-Wen, C., Wei-Jye, W., 2005. Preparation of nanosized iron oxide and its application in low temperature CO oxidation. Journal of Nanoparticle Research 7, 249–263. Kitis, M., Lozier, J.C., Kim, J.H., Mi, B.X., Marinas, B.J., 2003. Microbial removal and integrity monitoring of RO and NF membranes. Journal of the American Water Works Association 95 (12), 105–119. Lead, J., Wilkinson, K., Starchev, K., Canonica, S., Buffle, J., 2000. Determination of diffusion coefficients of humic substances by fluorescence correlation spectroscopy: role of solution conditions. Environmental Science and Technology 34, 1365–1369. Li, Q., Snoeyink, V., Marinas, B., Campos, C., 2003. Elucidating competitive adsorption mechanisms of atrazine and NOM using model compounds. Water Research 37, 773–784. Lukasik, J., Cheng, Y.F., Lu, F.H., Tamplin, M., Farrah, S.R., 1999. Removal of microorganisms from water by columns containing sand coated with ferric and aluminum hydroxides. Water Research 33 (3), 769–777. Nasser, A.M., Paulman, H., Sela, O., Ktaitzer, T., Cikurel, H., Zuckerman, I., Meir, A., Aharoni, A., Adin, A., 2006. UV Disinfection of Wastewater Effluents for Unrestricted Irrigation. IWA Publishing, pp. 83–88. Nguyen, T.H., Elimelech, M., 2007. Adsorption of plasmid DNA to a natural organic matter-coated silica surface: kinetics, conformation, and reversibility. Langmuir 23, 3273–3279. Parashar, U.D., Gibson, C.J., Bresee, J.S., Glass, R.I., 2006. Rotavirus and severe childhood diarrhea. Emerging Infectious Diseases 12 (2), 304–306. Penrod, S.L., Olson, T.M., Grant, S.B., 1996. Deposition kinetics of two viruses in packed beds of quartz granular media. Langmuir 12 (23), 5576–5587. Pham, M., Nguyen, E.A., 2009. Deposition kinetics of bacteriophage MS2 to natural organic matter: role of divalent cations. Journal of Colloid and Interface Science 338, 1–9. Rolsma, M.D., Gelberg, H.B., Kuhlenschmidt, M.S., 1994. Assay for evaluation of rotavirus-cell interactions – identification of an enterocyte ganglioside fraction that mediates group-a porcine rotavirus recognition. Journal of Virology 68 (1), 258–268. Rolsma, M.D., Kuhlenschmidt, T.B., Gelberg, H.B., Kuhlenschmidt, M.S., 1998. Structure and function of a ganglioside receptor for porcine rotavirus. Journal of Virology 72 (11), 9079–9091. Rouquerol, F., Rouquerol, J., Sing, K., 1999. Adsorption by Powders and Porous Solids: Principle, Methodology and Application. Academic Press, New York. Ruiz, M., Charpilienne, A., Liprandi, F., Gajardo, R., Michelangeli, F., Cohen, J., 1996. The concentration of Ca21 that solubilizes outer capsid proteins from rotavirus particles is dependent on the strain. Journal of Virology 70 (8), 4877–4883. Ryan, J., Elimelech, M., Ard, R., Harvey, R., Johnson, P., 1999. Bacteriophage PRD1 and silica colloid transport and recovery in an iron oxide-coated sand aquifer. Environmental Science and Technology 33, 63–73. Ryan, J., Harvey, R., Metge, D., Elimelech, M., Pieper, A., 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. Van Duin, J., 1988. The Bacteriophages. Plenum, New York. Wegmann, M., Michen, B., Graule, T., 2008a. Nanostructured surface modificationofmicroporousceramicsforefficientvirusfiltration. Journal of the European Ceramic Society 28 (8), 1603–1612. Wegmann, M., Michen, B., Luxbacher, T., Fritsch, J., Graule, T., 2008b. Modification of ceramic microfilters with colloidal zirconia to promote the adsorption of viruses from water. Water Research 42 (6–7), 1726–1734. Wyn-Jones, A., Sellwood, J., 2001. Enteric viruses in the aquatic environment. Journal of Applied Microbiology 91, 845–863. You, Y., Vance, G., Sparks, D., Zhuang, J., Jin, Y., 2003. Sorption of MS2 bacteriophage to layered double hydroxides: effects of reaction time, pH, and competing anions. Journal of Environmental Quality 32, 2046–2053. You, Y.W., Han, J., Chiu, P.C., Jin, Y., 2005. Removal and inactivation of waterborne viruses using zerovalent iron. Environmental Science and Technology 39 (23), 9263–9269. Yuan, B.L., Pham, M., Nguyen, T.H., 2008. Deposition kinetics of bacteriophage MS2 on a silica surface coated with natural organic matter in a radial stagnation point flow cell. Environmental Science and Technology 42 (20), 7628–7633. Yue, Z., Mangun, C., Economy, J., 2001. Removal of chemical contaminants from water to below USEPA MCL using fiber glass supported activated carbon filters. Environmental Science and Technology 35 (13), 2844–2848. 5208 w a t e r r e s e a r c h 4 3 ( 2 0 0 9 ) 5 1 9 8 – 5 2 0 8

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