Improved Virus Removal in Ceramic Depth Filters Modified with MgO

Jan 3, 2013 - Ceramic filters, working on the depth filtration principle, are known to improve ... Recently, it was shown that the addition of positiv...
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Improved Virus Removal in Ceramic Depth Filters Modified with MgO Benjamin Michen,*,†,‡ Johannes Fritsch,§ Christos Aneziris,‡ and Thomas Graule†,‡ †

Laboratory for High Performance Ceramics, EMPA, Swiss Federal Laboratories for Materials Science and Technology, Ueberlandstrasse 129, CH-8600 Duebendorf, Switzerland ‡ Institute for Ceramics, Glass and Construction Materials, Technical University Bergakademie Freiberg, Agricolastrasse 17, D-09596 Freiberg, Germany § Technology and Management Faculty, University of Applied Sciences Ravensburg−Weingarten, Doggenriedstrasse, D-88241 Weingarten, Germany S Supporting Information *

ABSTRACT: Ceramic filters, working on the depth filtration principle, are known to improve drinking water quality by removing human pathogenic microorganisms from contaminated water. However, these microfilters show no sufficient barrier for viruses having diameters down to 20 nm. Recently, it was shown that the addition of positively charged materials, for example, iron oxyhydroxide, can improve virus removal by adsorption mechanisms. In this work, we modified a common ceramic filter based on diatomaceous earth by introducing a novel virus adsorbent material, magnesium oxyhydroxide, into the filter matrix. Such filters showed an improved removal of about 4-log in regard to bacteriophages MS2 and PhiX174. This is explained with the electrostatic enhanced adsorption approach that is the favorable adsorption of negatively charged viruses onto positively charged patches in an otherwise negatively charged filter matrix. Furthermore, we provide theoretical evidence applying calculations according to Derjaguin− Landau−Verwey−Overbeek theory to strengthen our experimental results. However, modified filters showed a significant variance in virus removal efficiency over the course of long-term filtration experiments with virus removal increasing with filter operation time (or filter aging). This is explained by transformational changes of MgO in the filter upon contact with water. It also demonstrates that filter history is of great concern when filters working on the adsorption principles are evaluated in regard to their retention performance as their surface characteristics may alter with use. Both technologies are based on the depth filtration principle that allows for higher throughput during filtration and less fouling when compared to surface filtration and its sizeexclusion principle. Bearing in mind the drawbacks of surface filtration, it cannot be neglected that ceramic filters working on the size-exclusion principle have shown virus retention of 99.9999%.7 However, such high virus removals have been also achieved with depth filters based on multiwalled carbon nanotubes 8 or surface charge modified ceramic depth filters.16,17 In this study, we focus on ceramic filters that have been shown to remove large-sized microorganisms such as protozoa and bacteria.9 However, these filters fail to remove viruses, the smaller-sized group of pathogens, to a sufficient level.10 Viruses are difficult to capture in depth filters that usually have pore sizes larger than the viral dimension. This drawback of depth filtration has been recognized by the community, and some attempts have been made with which virus removal in depth filters could be improved. Those achievements are based on the

1. INTRODUCTION Although water contaminated with human pathogenic viruses has been the source of numerous outbreaks worldwide, access to safe drinking water is a problem more frequently met in less developed nations.1 Besides hepatitis A and E, an increasing number of viral gastroenteritis epidemics have been reported recently.2 Thus, viruses become more and more recognized as an emerging issue related to water transmitted diseases. In order to purify water from contaminants, such as viruses for instance, a variety of methods are available. These technologies often rely on multistage treatment, electric energy supply, and trained personnel, making water treatment too expensive for less developed countries.3 This and the fact that problems with water are expected to grow worse in the future specifies our need to develop novel methods to purify water at lower cost and with less energy.4 One promising approach is decentralized water treatment in catastrophic areas or less developed countries.5 Decentralized technologies, in particular water treatment methods at the point-of-use, have been reviewed6 in regard to criteria that are important to developing countries. For example, these are the ease of use, cost and supply chain of water treatment technologies, as well as the quantity and quality of purified water produced. Thereby, ceramic and biosand household water filters demonstrated the best performance. © 2013 American Chemical Society

Received: Revised: Accepted: Published: 1526

September 11, 2012 December 28, 2012 January 2, 2013 January 3, 2013 dx.doi.org/10.1021/es303685a | Environ. Sci. Technol. 2013, 47, 1526−1533

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2. EXPERIMENTAL SECTION 2.1. Ceramic Filters. The base filters chosen were tubular ceramic elements (length: 119 mm; outer diameter: 50 mm; inner diameter: 35 mm) that consist of a proprietary mixture of diatomaceous earth and layered silicates and are manufactured using an extrusion process followed by firing at temperatures over 1000 °C. Details on composition, production steps, and characteristics of the base filter have been the subject of previous studies.9,10 Such base filters have been modified in this work by adding MgO (MgO light, Fluka) into the extrusion mixture prior to forming, drying, and firing the filter. Thereby, the recipe was identical with that of the base filter, except that a certain mass fraction of diatomaceous earth (type SSC) was exchanged with MgO powder. The amount of MgO introduced into the filter varied, and the specification is given as weight percent. 2.2. Physical and Chemical Characterization. Ceramic filters were characterized using mercury intrusion porosimetry to collect information on filter porosity (open porosity) and pore size. Measurements were performed using the combination of Pascal 140 and Pascal 440 (ThermoQuest Italia S.p.A.) to gain intrusion data within a pressure range from 0.1 kPa to 400 MPa that allowed the investigation of pore diameters in the range from 116 to 0.0036 μm, respectively. The specific surface area of filters and the MgO powder was determined by the adsorption of nitrogen at 77 K according to the method of Brunauer−Emmett−Teller (BET; SA3100, Beckman−Coulter, USA). Samples were dried at 200 °C and degassed with nitrogen for 3 h prior to BET measurements. Scanning electron microscopy (SEM; S-4800, Hitachi, Japan) was used to image ceramic samples. All samples were sputtered with a layer of a conductive Au−Pd alloy to avoid sample charging during SEM examination. ζ potential measurements were performed by microelectrophoresis using a Zetasizer Nano ZS (Malvern Instruments, UK). Experiments were driven by the Dispersion Technology Software (Version 5.03) that calculated the ζ potential based on the measured electrophoretic mobility. Clear disposable capillary cells (DTS 1060, Malvern Instruments, UK) were used and connected with the autotitrator MPT-2 (Malvern Instruments, UK) in order to determine the ζ potential as a function of pH. NaOH and HCl solutions of 0.1 and 0.01 M were used as titrants to adjust the pH. Filters needed to be destroyed to obtain a fine powder: To avoid contamination of the sample, two filter fracture surfaces were ground on each other to produce powders. These powders were diluted in 4 mM NaCl and strongly shaken. Sedimentation of the sample was allowed for 15 min, and the supernatant was collected for ζ potential measurements. The flow rate of the elements was determined by forcing tap water at 3 bar and 25 °C through the filter. Thereby, a particular effluent volume was collected, and the corresponding time was recorded. Experiments were usually performed at least three times, and results are expressed as the mean value with the corresponding standard deviation. The crystallographic structure and its chemical composition were investigated using an Xray diffraction (XRD) technique (X’Pert Pro MPD, PANalytical, the Netherlands). A scan from 2θ of 5° to 80° was performed with a step size of 0.0167° within a scan time of 150 min (Cu Kα radiation, 40 mA heating current, 45 kV beam potential). 2.3. Viruses. Here, two types of bacteriophages have been used to model the removal of human enteric viruses10,12−17 in

electrostatic enhanced adsorption approach: This is the favorable adsorption of viruses, which carry a net negative surface charge in the aquatic environment,11 onto positively charged adsorbent materials. Thereby, hydrated iron oxide surfaces (oxyhydroxides) have shown to increase virus removal significantly when the material was implemented in a filter matrix composed of glass fibres12 or added to a biosand filter.13 Also, iron particles, which transform upon corrosion to iron oxyhydroxides, showed an improved removal of viruses in batch and column experiments.14 In another study, the net negative surface charge of sand was modified by coating it with positively charged iron oxyhydroxide as well as aluminum oxide. The removal of viruses was then studied in filtration columns. When compared to uncoated sand, the virus removal significantly increased in columns containing coated sand.15 Likewise, the modification of tubular ceramic filters was achieved by coating the internal surface of the filter with positively charged hydrated oxides of yttrium16 and zirconium17 increasing virus retention from 10 may even increase electrostatic interactions between virus and filter material due to a larger difference in net charges and thus higher electrostatic forces involved. On the basis of that, we selected magnesia, or MgO, as a potential adsorbent material for viruses in this study. The surface of MgO in contact with water is promptly transformed into its hydroxide Mg(OH) 2,20 and thus, magnesium oxyhydroxide is formed that consists of a MgO core and hydroxides covering its surface/interface. This material has an IEP in the basic regime at pH 1219 making it a promising material for enhanced virus removal. A few studies support our approach, since Mg(OH)2 has been used to concentrate poliovirus21 and several bacteriophages22 from water by adsorption mechanisms used in flocculation. Also, MgO has been studied as an additive to enhance virus removal as a method of groundwater protection.23 However, to the best of our knowledge, magnesium oxyhydroxide has never been implemented into a (depth) filter with the goal to improve virus removal in water treatment. Hence, this study investigates the modification of ceramic depth filters based on diatomaceous earth by the incorporation of MgO into the filter matrix. The introduced positively charged surface sites (patches) are thought to improve virus capture in filtration experiments. This is of great interest not only because it would offer an alternative adsorbent material for viruses with a higher IEP but because it is also readily available, not harmful, and of low cost. Moreover, magnesium oxyhydroxide has additional benefits in water treatment where it may be used to remove toxic metal ions, such as Ni,24 Zn, and Mn.25 1527

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Table 1. Some Characteristics of the MgO-Modified Depth Filters filter type

BET (m2/g)

mean pore diameter (μm)

porosity (v%)

flux (m/h)

0 wt % MgO 10 wt % MgO 15 wt % MgO 20 wt % MgO 30 wt % MgO

2.1 3.2 3.8 4.6 6.7

3.2 2 ND 1.6 1.4

64 71.5 ND 73.5 74.6

6.8 6.1 5.4 4.5 ND

ceramic depth filters. We chose enterobacteria phage MS2 (MS2; IEP = 3.5; diameter = 25 nm) and enterobacteria phage PhiX174 (Phi; IEP = 6.6; diameter = 26 nm) to investigate virus adsorption. The bacteriophages MS2 (DSM 13767) and Phi (DSM 4497) were obtained from the German Collection of Microorganisms and Cell Cultures (DSMZ, Germany). We used liquid propagation methods for all phages including purification of virus stocks by washing, centrifugation, and dialysis. The propagation of bateriophages was carried out with two different strains of Escherichia coli obtained from the DSMZ. The two strains were DSM 5210 and DSM 13127 for the replication of F-specific phage MS2 and the somatic phage Phi, respectively. The enumeration took place by counting plaques on lawns of bacteria in Petri dishes. The bacteria strains used for the specific enumeration of the phages MS2 and Phi were obtained from the American Type Culture Collection (ATCC): E. coli HS(pFamp)R/Famp (ATCC 700891) and E. coli CN-13 (ATCC 700609) for MS2 and Phi, respectively. Details on propagation, purification, and enumeration have been reported earlier.10 2.4. Filtration Experiment. Ceramic filters were clamped in a mount and tested for leaks with a bubble-point test before a filtration experiment was carried out. All filters were flushed with deionized water at 3 bar for at least 3 min in order to prevent artifacts originating from interactions between dust particles left from the machining of the filter and/or air−water interfaces at nonwetted pores.9,10 Wet filters were subjected to retention tests in a laboratory-scaled experimental setup that was composed of a filter housing sealing the mounted ceramic depth filter. A tube connected the housing with a 50 L stainless steel pressure vessel containing the test water. Compressed air was used to force the water through the ceramic at a pressure of 3 bar. The test waters used here were as follows: (1) Deionized water (conductivity 4 were measured before the retention dropped to a LRV = 2.5 after 200 L of test water had passed through the filter. A retention of approximately LRV = 2.5 remained until 400 L of effluent had passed through the filter, at which point the performance began to decrease gradually. Several attempts have been made in order to better understand these puzzling changes in filter performance that are in contradiction with conventional adsorption filters: Since Mg(OH)2 is slightly soluble in water and can alter its pH, it is reasonable to monitor the pH in the effluent of modified filters. This may be important because viruses may become inactivated in a basic environment and also in order to fulfill the requirements for drinking water standards in which the pH should be in the range from 5 to 9 for human drinking purposes. Indeed, the pH in the effluent of MgO-modified filters was found to be considerably higher (up to pH > 9) than the pH value in the influent. It is worth mentioning here that the pH shift in the effluent was only observed following a filter operation stop and the change became less pronounced with an increasing number of stops (data not shown). The very first effluents (less than 1 L) showed pH values above pH 9 and could not be considered appropriate for drinking water. However, the change in pH became less pronounced with larger effluent volumes. After 1 L, the filtered water was adequate for human drinking purpose, see Figure S-6 in the Supporting Information. Regarding the potential inactivation of the phage MS2 in the basic regime, the titer reduction at various pH values was determined in a previous study.10 Our results were in agreement with those by Feng et al.29 where a reduction of MS2 titer was below 1 LRV at pH levels from 9 to 10. Thus, it is unlikely that the improved MS2 removal in the 1529

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Figure 3. (a) MS2 removal conducted in tap water on a virgin filter element containing 15 wt % of MgO. (b) Different pH shifts in the effluent of a virgin and a nonvirgin filter element. (c) Reduction in flow rate through a virgin filter element as a function of time.

Figure 4. Retention of bacteriphoges MS2 and Phi conducted in soft water at pH 7. (a−c) Results obtained using a filter element that has been subjected to three filtration tests after 0, 75, and 131 days, respectively.

MgO-containing filter was due to a chemical inactivation induced by basic pH, in particular, as water samples for virus enumeration were taken after a minimum of 2 L had passed the filter. The fact that this pH shift has been observed can be linked to the loss of the adsorbent material induced by its dissolution. However, this would still not explain the course of the data points in Figure 2, because the loss of adsorbent material would be expected to gradually decrease with increasing effluent volume. Consequentially, one would expect the adsorption of bacteriophages to correlate with this gradual decrease. This is in contradiction with the plateau at LRV = 2.5 for the 20 wt % modified filter and also with the increase in LRV from 2.1 to 2.7 with the 15 wt % MgO-containing filter. These filters possibly underwent changes in their characteristics that have not yet been considered. If, in addition to dissolution, another process occurred that improved the retention performance, this could account for the previously observed complex courses. Such a process could be the (re)formation of attractive magnesium oxyhydroxide sites in the filter. It is thus proposed that the dissolution of magnesium (oxy-)hydroxide as well as its (re)formation are the two processes that accounted for the puzzling changes to the retention curves. Thus, it is hypothesized that filter history is of great concern when filters are evaluated in regard to their retention performance as their surface characteristics may alter with use. 3.2.1. Investigating the Effect of Filter Aging on the Virus Removal Performance. Up to now, all modified filter candles had been in contact with water prior to the performance of any virus retention test, for example, when the flow rate was measured. During the time of first water contact and the virus

retention test (at least two days), the novel component, MgO, in the modified filter may have partly reacted to form magnesium oxyhydroxide that is thought to offer virus adsorption sites. To strengthen our hypothesis, we investigated further the formation of magnesium oxyhydroxides using virgin filter elements (a filter element after production that had not been in contact with water). At the outset, a virgin filter candle containing 15 wt % MgO was subjected to a continuously performed MS2 retention test. This test was carried out within one day, with the introduction of alternating periods of virusloaded tap water and tap water free of viruses. The MS2 retention over the effluent volume is shown in Figure 3a. While the retention of bacteriophage MS2 by the nonvirgin filter, also modified with 15 wt % MgO, used in the previous experiment (Figure 2) was between 2 and 3 LRV in the first 120 L, the virgin filter element showed significantly less retention with LRV < 1 over 300 L. This low virus removal and the fact that the effluent pH of the virgin filter was not altered in the way it had been recorded for the modified filter in the previous experiment (see Figure 3b) relate improved phage removal with the dissolution of Mg(OH)2. However, prior to its dissolution, it must be formed in the filter, presumably as part of the oxyhydroxide compound. This confirms the hypothesis that removal takes place at adsorption sites originating from the transformation to magnesium oxyhydroxide. Consequentially, the transformation in the virgin filter was not achieved during the time in which the test was performed (approximately 360 min). However, the slight increase in MS2 removal shown in Figure 3a over the effluent volume indicated that the formation had begun to take place. Further evidence for the transformational change was obtained by the observation of the flow rate 1530

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through the virgin filter over time, as shown in Figure 3c. While the filter showed a constant flow rate during the time when the virus retention test was performed, it decreased significantly after approximately 1000 min. During the time of this experiment (approximately 10 000 min), the filter was always wet although it underwent operational stops. The decrease in flow rate was also observed with the 15 and 20 wt % modified filters (data not shown) in the previously performed MS2 retention test shown in Figure 2. This reduction in flow rate may be explained with the volume expansion of MgO as it transformed into Mg(OH)2. Moreover, after a total of 450 L of tap water passed through the filter, it was subjected to another MS2 retention test one week after the first retention experiment. More than 50 L spiked with MS2 phages was forced through the filter, and no single phage could be detected in eight effluent samples within these 50 L. Due to the detection limit of the enumeration method, the retention of MS2 was LRV > 4.9 (data not shown). In order to systematically evaluate the change in filter characteristics of a virgin element, an additional experiment was performed: A filter candle containing 20 wt % MgO was repeatedly subjected to a defined test cycle. This cycle comprised flushing the filter candle with 5 L of deionized water. Subsequently, the filter was checked for the removal of both bacteriophages MS2 and Phi in soft water at pH 7. After the retention test was conducted, the filter was allowed to dry under ambient conditions, that is, room temperature and humidity of approximately 50%, for several weeks before the filter element was once again subjected to the test cycle. The removal of phages as a function of effluent for three cycles is shown in Figure 4a−c. Green rectangles and red circles refer to MS2 and Phi, respectively. Dashed lines in the corresponding color show the detection limit in each experiment. The low removal of both phages in the first test is in agreement with the previous results in Figure 3a and supports as well the hypothesis that the necessary transformation had not been accomplished. The results of the second test (Figure 4b) show that a transformation had occurred and explains the significant improvement in phage reduction. While for MS2, a LRV > 4.2 was measured in the first 13 L, and the retention was lower for Phi with a maximum LRV = 3.3 at 5 L of effluent. However, the removal of both phages was found to decrease after 20 L, indicating that the removal mechanism became exhausted, that is, the available adsorption sites were blocked. Figure 4c shows the results of the third test where the filter performance was further improved with LRV > 3.6 for MS2 at effluent volumes > 40 L (detection limit at LRV = 3.6). Bacteriophage Phi showed improvement in retention with a maximum LRV = 4 after which the LRV decreased slightly to LRV = 3 at 40 L. The fact that MS2 was removed consistently at LRV > 3.6 over 40 L of effluent indicated a more favorable retention of MS2 compared to Phi. This preferred removal of MS2 was also observed in the second test (Figure 4b). The results of the three cycles shown in Figure 4 are summarized in Figure 5. Here, the LRVs of MS2 and Phi after 20 L of effluent are plotted over the number of filtration tests performed. Also, the reference filter (containing no additional MgO) has been subjected to three test cycles in which one filter element was repeatedly tested for MS2 and Phi removal. The figure reveals that, in contrast to the MgO-modified filter, no enhanced virus removal occurred with the base filter. This clearly demonstrated that virus removal in the MgO-modified depth filter was improved relative to the reference filter.

Figure 5. Comparison of MgO-modified depth filter with the reference filter. MS2 and Phi retention after 20 L of effluent recorded for three in sequence conducted filtrations tests (see Figure 4). Removal was investigated in soft water at pH 7.

3.2.2. Discussion on the Removal Mechanisms. It has been shown that the introduction of MgO into depth filters can significantly improve the retention of bacteriophages MS2 and Phi by more than 4 LRV, or 99.99%, compared to the reference filter. However, the virgin filter element is not capable of removing infectious viruses. After the filter has been in operation, the virus retention efficiency is considerably improved accompanied by other changes in filter characteristics, for example, the drop in flow rate. Thus, the reaction of MgO within the depth filter might be hampered by mechanical forces during volume expansion to form magnesium oxyhydroxide, and MgO grains might be covered in a way that viruses may not access the adsorbent surface. In order to remove bacteriophages in the MgO-modified filter candles, a change in filter surface characteristics associated with waterbased reactions needs to take place. These changes have been shown to alter virus removal in a complex manner related to filter operation history. The changes presumably involve the formation of magnesium oxyhydroxides originating from the bare MgO that was introduced into the filter matrix. Thus, positively charged patches (adsorption sites) on the magnesium oxyhydroxides are suspected to favor virus adsorption according to the electrostatic enhanced adsorption approach and to increase the attachment efficiency. This is endorsed by calculations based on Derjaguin−Landau−Verwey−Overbeek (DLVO) theory. We performed the calculations using previously reported equations,10 and more details are reported in the Supporting Information. The results are given in Figure 6, where the energy−distance curves between both phages and the magnesium oxyhydroxide surface are plotted. The calculations show no energy barrier in soft water at pH 7 for both MS2 and Phi. Thus, the figure reveals only attractive interactions for both phages, whereas MS2 experiences attraction at larger distances relative to Phi. This could explain the preferred removal of MS2 compared to Phi in Figure 4b,c. On the other hand, the previously proposed steric barrier of Phi10 could also explain a preferred retention of MS2 relative to Phi. However, the retention of bacteriophages in MgO-modified filters was strongly influenced by transformational changes in filter characteristics dependent on operation history or filter aging. Because these changes influence the filter performance with operation time, such filters are not recommended for drinking water production due to significant variations in virus 1531

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removal. Moreover, the filter may alter the pH in the effluent to values above pH 9, which does not fulfill drinking water regulations. The pH shift occurs in the first effluent volumes and is influenced by the buffering capacity of the test water. Nevertheless, magnesium oxyhydroxide has a great potential to remove viruses from water due to its high IEP, availability, and low cost. If operated in a continuous flow-through mode, such filters would not suffer from a significant pH shift. Also, choosing a more suitable filter matrix into which MgO is introduced may hamper cracking of filter elements and would allow introducing higher loads of adsorbent material. This would be expected to increase the adsorption activity. Thus, we propose to investigate the great potential of magnesium oxyhydroxides and its virus removal activity for (decentralized) water treatment. Moreover, we want to highlight the importance of carrying out long-term filtration experiments, in particular with filters working on the adsorption principle, in order to evaluate whether such filters retain their surface characteristics with use and therewith their removal activity. Such long-term experiments are of utmost importance when the lifetime of any filters working on the adsorption principle need to be determined. However, the filter’s lifetime will be affected by the presence of substances that compete for the available adsorption sites, such as natural organic matter. These substances are known to reduce the removal efficiency of viruses in depth filters.16

ASSOCIATED CONTENT

S Supporting Information *

Further physical and chemical characterization of MgOmodified ceramic filters including pore size distribution, SEM, and XRD; the surface charge of MgO measured in the aquatic environment; dissolution of Mg(OH)2 and pH shift; DLVO calculations; and references. This material is available free of charge via the Internet at http://pubs.acs.org.

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REFERENCES

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Figure 6. Energy−distance curves for MS2 and Phi approaching the magnesium oxyhydroxide surface according to DLVO theory.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by EMPA internal funding. Thanks are extended to Mrs. Natasa Rittiner for her valuable contribution. 1532

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