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Applied and Environmental Microbiology, July 2000, p. 2914-2920, Vol. 66, No. 7
Department of Microbiology and Cell Science,
University of Florida, Gainesville, Florida 32611-0700
Received 15 March 1999/Accepted 11 April 2000
We investigated the direct and indirect effects of mono-, di-, and
trivalent salts (NaCl, MgCl2, and AlCl3) on the
adsorption of several viruses (MS2, PRD-1, The effects of salts on virus
adsorption to microporous filters have been studied for many years and
have been discussed in several reviews (4, 13, 16, 17, 28).
In previous studies, the researchers concluded that addition of
aluminum ions (or magnesium ions) enhanced viral adsorption to
microporous filters, and from these results it was concluded that the
presence of salts is necessary for optimum viral adsorption to the
filters (4, 13, 16, 17, 27, 28). However, we found two
problems with the earlier studies. First, relatively few viruses and
few microporous filters were studied. Much of the information was
information concerning the adsorption of poliovirus to
nitrocellulose filters (Millipore filters). However, due to
recent developments in filter technology, new filters that have
substantially different properties than the filters previously studied
are currently being used. Therefore, it is necessary to evaluate the
effects of salts on these filters.
Second, previous studies on the effects of salts on virus adsorption
did not distinguish between direct and indirect effects of the salts
that influenced viral adsorption. The direct effects that have been
proposed include formation of salt bridges between the viruses and the
filters (16) and alteration of the charge of a filter
(14). The indirect effects include (i) a decrease in the pH
due to addition of aluminum salts to purified water (28);
(ii) the formation of flocs that adsorb viruses and are then physically
trapped by the filters (9, 28); and (iii) the reaction
between aluminum ions and humic materials that interfere with virus
adsorption (10, 25).
In order to better understand the forces involved in viral adsorption
to solids, we investigated the adsorption of four viruses to four
commercially available filters having different compositions and
different physical characteristics. Two of the filters used in this
study (Filterite and 1MDS filters) are currently used for recovering
viruses from water (1, 2). The Filterite filters have a net
negative charge at pH values near neutrality, in contrast to the 1MDS
filters, which are positively charged or have a slight negative charge
at similar pH values (14, 24). Nitrocellulose filters
(Millipore HA filters) also have a net negative charge at pH 7 (14) and have been used in studies on virus adsorption and
to recover viruses from water (6, 7, 12, 28). Cellulose
filters (Whatman filters) were included as an example of filters that
poorly adsorb viruses. These filters are made from material that is
electronegative at pH 7 (26) and have little ability to
adsorb viruses unless they are modified (11).
Mono- and multivalent salts were used at different pH values, and
compounds that have been shown to disrupt hydrophobic interactions were
also used. In addition, the effects of different concentrations of
aluminum and the effects of different concentrations of magnesium on pH
and viral adsorption, respectively, were studied. The previously described direct and indirect effects were minimized by controlling flocculation and pH by filtering and buffering. All virus stocks and
salt solutions were prefiltered through 0.2-µm-pore-size filters prior to each experiment to reduce the effects of aggregation and
flocculation. The pH was monitored and controlled, and only purified
water was used. Under these conditions, magnesium chloride was found to
promote virus adsorption, to interfere with virus adsorption, and to
have little or no effect on virus adsorption, depending on the virus
and the microporous filter tested. The most consistent effect of sodium
chloride and aluminum chloride on virus adsorption was to interfere
with virus adsorption to 1MDS filters.
Filtration of samples.
All viral stocks and solutions were
prefiltered through a 0.2-µm-pore-size filter (Millipore GS;
Millipore Corp., Bedford, Mass.) that had been prewashed with 20 ml of
deionized water before use.
Viruses.
The phages used in this study, their isoelectric
points (1), and their hosts are as follows: MS2 (=
ATCC 15597-B1), pl 3.9, Escherichia coli C-3000
(= ATCC 15597); Microporous filters.
The flowing microporous filters were
used: Millipore HA filters (nitrocellulose; Millipore Corp.); Filterite
0.20-µm-pore-size filters (bound fiberglass; Filterite Corp.,
Timonium, Md.); Whatman no. 5 filters (cellulose; Fischer Scientific,
Pittsburgh, Pa.); and 1MDS filters (charge-modified fibers; AMF Cuno,
Meridan, Conn.). The Filterite and 1MDS filters were purchased as
cartridge filters. These filters were broken down, and smaller filters
were cut from the filter material. The Millipore, Filterite, and
Whatman filters are negatively charged at pH values near neutrality;
the 1MDS filters are positively or slightly negatively charged at the
same pH values (14, 19, 24, 26).
Solutions.
Solutions of sodium chloride, magnesium chloride,
aluminum chloride, urea, and Tween 80 were prepared with a buffer
solution (0.02 M imidazole-0.02 M glycine, unless otherwise
indicated). The solutions were adjusted to the required pH by adding 1 M NaOH or 1 M HCl. Tap water was dechlorinated by adding 10 mg of
sodium thiosulfate per liter. Deionized water (>15 M Aluminum chloride and magnesium chloride titration
experiments.
For aluminum chloride and magnesium chloride
titration experiments (Fig.
1 through
3), aliquots of a 1.00 M aluminum
chloride or 1.00 M magnesium chloride solution were added to a 0.002 M glycine-0.002 M imidazole solution or to purified water to obtain the
desired concentrations. Since the concentrations of salts used in these
experiments were lower than the concentrations used in other
experiments, a lower concentration of buffer was used to reduce
interference with the metallic ions by buffer ions.
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Influence of Salts on Virus Adsorption to
Microporous Filters
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
X174, and poliovirus 1)
to microporous filters at different pH values. The filters studied
included Millipore HA (nitrocellulose), Filterite (fiberglass), Whatman
(cellulose), and 1MDS (charged-modified fiber) filters. Each of these
filters except the Whatman cellulose filters has been used in virus
removal and recovery procedures. The direct effects of added salts were considered to be the effects associated with the presence of
the soluble salts. The indirect effects of the added salts were
considered to be (i) changes in the pH values of solutions and (ii) the
formation of insoluble precipitates that could adsorb viruses and be
removed by filtration. When direct effects alone were considered, the salts used in this study promoted virus adsorption, interfered with
virus adsorption, or had little or no effect on virus adsorption, depending on the filter, the virus, and the salt. Although we were able
to confirm previous reports that the addition of aluminum chloride to
water enhances virus adsorption to microporous filters, we found that
the enhanced adsorption was associated with indirect effects rather
than direct effects. The increase in viral adsorption observed
when aluminum chloride was added to water was related to the decrease
in the pH of the water. Similar results could be obtained by adding
HCl. The increased adsorption of viruses in water at pH 7 following
addition of aluminum chloride was probably due to flocculation of
aluminum, since removal of flocs by filtration greatly reduced the
enhancement observed. The only direct effect of aluminum chloride on
virus adsorption that we observed was interference with adsorption to
microporous filters. Under conditions under which hydrophobic
interactions were minimal, aluminum chloride interfered with virus
adsorption to Millipore, Filterite, and 1MDS filters. In most cases,
less than 10% of the viruses adsorbed to filters in the presence
of a multivalent salt and a compound that interfered with
hydrophobic interactions (0.1% Tween 80 or 4 M urea).
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
X174 (= ATCC 13706-B1), pl 6.6, E. coli ATCC 13607; and PRD-1, pl 4.2, Salmonella
typhimurium ATCC 19585. Numbers of phage PFU were determined by
using the appropriate hosts and a soft-agar overlay (23).
Poliovirus 1 (pI, approximately 4 and 7 [13]) was
grown on BGM cells, and the number of poliovirus PFU was determined by
an agar overlay method (22).
-cm) was
obtained from a Barnstead NANOpure II unit.
View larger version (21K):
[in a new window]
FIG. 1.
Influence of magnesium chloride concentration on
adsorption of poliovirus 1 to 1MDS and Millipore HA filters at pH 7.
View larger version (19K):
[in a new window]
FIG. 2.
Influence of magnesium chloride concentration on
adsorption of poliovirus 1 to 1MDS and Millipore HA filters at pH
3.5.
View larger version (18K):
[in a new window]
FIG. 3.
Influence of aluminum chloride concentration on
adsorption of poliovirus 1 to 1MDS and Millipore HA filters at pH
3.5.
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Experimental procedure.
Most experiments were conducted at
pH 7.0 or 3.5. The lower pH (pH 3.5) was selected since it has been
used in several other studies and is the recommended pH for recovering
viruses in water when Filterite filters are used (2, 3, 18,
27). Also, the aluminum salts used (at the concentrations used)
are soluble at pH 3.5. Aluminum salts were not used at pH 7 (Table
1 and 2)
since they are relatively insoluble and form flocs that can adsorb
viruses (8, 9). Viruses were added to solutions to obtain an
initial titer of approximately 105 PFU/ml. The viruses in
the solutions were assayed following dilution in 1% tryptic soy broth
(Difco) for phages or in minimal essential medium supplemented with 2%
fetal calf serum for poliovirus. In each case the dilution was
sufficient to raise the pH of the sample to approximately 7. To prevent
flocculation when experiments were performed with aluminum chloride, an
initial 1/10 dilution with deionized water was prepared, and then a
second dilution with the dilution media described above was prepared.
The filters used were 25-mm circles or filters cut into 25-mm circles
and placed into stainless steel filter holders. One layer of Millipore
HA filter material, two layers of Filterite filter material, two layers
of Whatman no. 5 filter material, or three layers of 1MDS filter
material were placed in each holder for the experiment. Each filter
preparation was first rinsed with 60 ml of deionized water. Then 25 ml
of the salt solution containing viruses was passed through each filter
by using a mechanical syringe infusion pump (Harvard Apparatus Co.,
Millis, Mass.) at a flow rate 1.5 ml/s. The filter effluents were
assayed for viruses, and the percentage removed was determined. A
portion of each sample that had not been passed through any filter was
assayed at the beginning and at the end of each experiment to determine
if the solutions inactivated the viruses. The numbers of viruses in the
unfiltered and filtered samples were used to determine the percentages
removed by the filters. Each experiment was performed in triplicate. In
addition, each experiment was performed at least twice. Therefore, each value reported below represents a mean based on at least six
determinations. The error associated with the values reported was less
than 
n, where n is the number of the
PFU counted. A statistical analysis of the data obtained (standard
deviations, slopes, correlation, and general t test
probabilities) was performed by using PSI-Plot software (Poly Software
International, Salt Lake City, Utah).
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Measurement of aluminum concentrations. Solutions were analyzed to determine total aluminum contents before and after filtration by workers at the Analytical Research Laboratory of the University of Florida.
Contact angle measurements. Contact angles for chloroform on filters were measured as previously described (21).
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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The effects of solutions of salts at pH 7 on the adsorption of the
viruses studied to the filters depended on the filter type and the salt
added (Table 1). In general, addition of salts increased the adsorption
of viruses to Millipore filters and interfered with the adsorption to
1MDS filters. Except for X174, the salts did not increase viral
adsorption to Whatman filters. Magnesium chloride greatly increased the
adsorption of poliovirus to Filterite filters; the salts had little or
no effect on adsorption of the phages tested to these filters.
The effects of buffer and buffer containing a salt (sodium chloride,
magnesium chloride, or aluminum chloride) at a concentration of 0.1 M
on adsorption of viruses at pH 3.5 are shown in Table 3. None of the salts affected viral
adsorption to Millipore or Whatman filters. More than 95% of the
viruses tested adsorbed to Millipore filters, and less than 10%
adsorbed to Whatman filters under all of the conditions tested;
however, the salts interfered with viral adsorption to 1MDS and
Filterite filters. The degree of interference depended on the virus and
the salt used. Aluminum chloride interfered with adsorption of viruses
to 1MDS filters more than magnesium chloride or sodium chloride
interfered with such adsorption. Only aluminum chloride interfered
significantly with virus adsorption to Filterite filters.
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The effect of the concentration of magnesium chloride on the adsorption of poliovirus to filters is shown in Fig. 1 and 2. At pH 7, increasing the concentration of magnesium chloride increased poliovirus 1 adsorption to Millipore HA filters but decreased poliovirus 1 adsorption to 1MDS filters (Fig. 1). At pH 3.5, increasing the concentration of magnesium chloride (Fig. 2) did not affect adsorption of poliovirus 1 to Millipore HA filters but decreased poliovirus 1 adsorption to 1MDS filters.
The effects of different concentrations of aluminum chloride on the adsorption of poliovirus to Millipore and 1MDS filters are shown in Fig. 3. Increasing the concentration of aluminum chloride had little effect on poliovirus adsorption to Millipore filters but interfered with adsorption of this virus to 1MDS filters.
The Millipore and 1MDS filters differed in hydrophobicity. The contact angle for chloroform on Millipore filters was 144.2 ± 3.2°, and the contact angle for chloroform on 1MDS filters was 151.8 ± 1.6°, which showed that the Millipore filters were more hydrophobic.
At pH 7 and in absence of salt ions, we observed little adsorption of poliovirus 1 in deionized water to Millipore HA filters (Fig. 4). As the concentration of aluminum chloride was increased, the adsorption of poliovirus increased. The pH values of the solutions also decreased as aluminum chloride was added. When the pH values of samples of deionized water were decreased by adding HCl, a similar trend in virus adsorption was observed. The decrease in the pH of the solution that was caused by the addition of aluminum chloride was sufficient to explain the observed increase in virus adsorption associated with the addition of aluminum chloride.
Adding urea in the absence of salt ions did not have a significant effect on viral adsorption to the filters at pH 7 (Table 2). However, viral adsorption was greatly reduced in the presence of both 4 M urea and a salt at a concentration of 0.1 M.
We observed a similar effect at pH 3.5; urea alone had little effect on
virus adsorption (Table 4). Adding 0.1 M
magnesium chloride or 0.1 M aluminum chloride to solutions of urea
reduced the adsorption of both MS2 and poliovirus 1 to the filters
tested. Tween 80 at a concentration of 0.1% had the same effect on
viral adsorption as 4 M urea had (data not shown). The effects of
prefiltering aluminum chloride solutions made with tap water before
viruses were added are shown in Table 5.
When a 0.0001 M aluminum chloride solution was prepared with tap
water at pH 7, viruses added to the solution were removed by a
Millipore HA filter. If the aluminum chloride solution was first passed
through a 0.2-µm-pore-size Millipore GS filter before the viruses
were added, then no significant viral adsorption to Millipore HA
filters was observed. The prefiltering step decreased the
concentration of aluminum chloride from 0.0001 M to less
than the detectable level (<0.00003 M). In contrast, no change
in the aluminum chloride concentration was observed following
filtration of 0.0001 M aluminum chloride solutions through the same
type of filter at pH 3.5 (where aluminum chloride is more soluble).
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In order to separate the effects of salt type from the effects of ionic
strength, we performed experiments in the presence of added salt at a
constant ionic strength. As shown in Table 6, magnesium chloride solutions were
better at promoting adsorption of MS2 and PRD-1 than sodium chloride
solutions at the same ionic strength were. Sodium chloride and
magnesium chloride both promoted adsorption of X174 to
nitrocellulose filters.
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Increasing the ionic strength of solutions of magnesium
chloride and sodium chloride to the ionic strength of aluminum
chloride decreased the adsorption of viruses to 1MDS filters
(Table 7). At a constant ionic strength
of 0.6, all of the salts significantly reduced the virus
adsorption that was observed in solutions containing buffer
alone. However, the greatest interference with adsorption was
observed with solutions of aluminum chloride.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Based on early studies on the influence of salts on virus adsorption, it was suggested that salts promote virus adsorption to microporous filters by promoting electrostatic interactions between the viruses and the filters. The possible mechanisms that were suggested to explain the observations made were salt bridging and charge neutralization of the filters. It was also suggested that the ability of salts to promote virus adsorption was related to the valence of the cation involved. Trivalent cations (Al3+) were better than divalent cations (Mg2+), which were better than monovalent cations (Na+), at promoting virus adsorption when the cations were used at the same concentration (4, 13, 16, 17, 27, 28).
In examining the early studies on the effects of salts on virus adsorption, we found three main problems. These were (i) the role of salts in promoting hydrophobic interactions was not always considered; (ii) the indirect effects of adding salts on the pH values of solutions and flocculation of the salts were not always determined; and (iii) few viruses and few filter types were studied. Below we discuss these problems in relation to our study.
Hydrophobic interactions. Previous studies on virus adsorption to microporous filters led to the suggestion that metal chelators could interfere with virus adsorption promoted by salts (14, 16, 17). Later studies showed that chelators, such as the citrate ion, did not elute viruses adsorbed to Millipore HA filters (7). In fact, chelators have been found to promote, rather than interfere with, virus adsorption to microporous filters (6). The study of Farrah (6) and other studies showed that increased virus adsorption to certain microporous filters in the presence of cations and anions was influenced by hydrophobic interactions (6, 12, 21). Therefore, the adsorption of MS2 and poliovirus 1 in the presence of salts to filters was best explained by the presence of hydrophobic interactions between the filters and the viruses. The effect of added magnesium chloride on virus adsorption was to strengthen hydrophobic interactions rather than electrostatic interactions (6).
In this study, urea had little effect on virus adsorption. This compound did not interfere with or promote adsorption of viruses to the filters tested at pH 7.0 or 3.5. In contrast, it greatly reduced virus adsorption when salts were present. The neutral detergent Tween 80 had an effect similar to that of urea, even though it was used at much lower concentrations. As discussed above, the salts probably promoted hydrophobic interactions and interfered with electrostatic interactions between the viruses and the filters (5, 12, 21).Indirect effects. Adding salts can change the pH of a solution or cause the formation of flocs, or salts can interact with organic material present in the solution. This is especially true for aluminum salts and makes determining the direct role of aluminum ions on virus adsorption difficult. As shown in Fig. 4, the effect of increasing the aluminum chloride concentration on virus adsorption reported by Wallis et al. (28) can be explained by the effect of aluminum chloride on the pH of the solution. Lowering the pH of deionized water by adding either aluminum chloride or an acid gave similar results for virus adsorption. It was not possible to reproduce exactly the effects of different concentrations of aluminum chloride on virus adsorption reported by Wallis et al. (28) since these authors did not report the pH values of the solutions which they used. However, the similarities are substantial, and the trend is identical.
Adding aluminum chloride to tap water or other solutions can produce flocs (8, 9). Removing these flocs from water may also remove viruses, and this process can be used to concentrate viruses from tap water. Previously, other authors (9, 27) have described removal of viruses in tap water following addition of aluminum chloride. This was more than likely the result of entrapment of flocs during filtration rather than enhancement of adsorption by soluble ions. As shown in Table 5, good viral removal is obtained if a pH 7 aluminum chloride solution (0.0001 M) containing viruses is passed through a Millipore filter. The ability to enhance removal is lost when the solution is prefiltered before the viruses are added and passed through the filter used to test for adsorption. It is likely that prefiltration removes flocs rather than soluble ions since passage of aluminum chloride solutions at pH 3.5 (in which aluminum chloride is more soluble) does not change the concentration of aluminum. Another indirect effect is the formation of complexes with humic matter in water by the cations added (10, 25). This may explain the requirement for adding aluminum chloride to water in virus concentration procedures (2, 3). It may also explain why the concentrations of aluminum chloride required for recovering viruses from organic matter-rich estuarine water (18) are higher than the concentrations required for recovering viruses from cleaner tap water.Viruses and filters studied. In many of the previous studies, adsorption of poliovirus and MS2 to Millipore HA filters was examined. These studies led to the conclusion that salts promote virus adsorption to microporous filters.
In this study, we used three filters composed of materials that are electronegative at pH values near neutrality (Millipore, Filterite, and Whatman filters) and one filter that is more electropositive under the same conditions (13, 21, 23). The difference between a negatively charged filter that is relatively hydrophobic (a Millipore HA filter) and a positively charged filter that less hydrophobic (a 1MDS filter) is clearly shown in Fig. 1 through 3. At pH 7, little adsorption of negatively charged viruses (above their isoelectric point) to a negatively charged filter (a Millipore filter) occurs. Increasing the salt concentration increases the hydrophobic interactions between the viruses and the Millipore filter, which increases adsorption. The salt also decreases electrostatic interactions between the viruses and the 1MDS filters, which decreases adsorption. The results obtained with 1MDS filters at pH 3.5 were similar. However, viruses adsorbed to Millipore filters at pH 3.5 under all of the conditions tested. Without salts, the viruses were positively charged (below their isoelectric points) and adsorbed to the negatively charged filters. Increasing the concentration of salts probably decreased the electrostatic interactions but also increased the hydrophobic interactions, so a constant, high percentage of the viruses adsorbed. The fact that the salts interfered with electrostatic interactions and increased hydrophobic interactions was evident when urea or Tween 80 was added and adsorption decreased substantially (Table 2 and 4). From the results of this and other studies (6, 12, 20, 21) we concluded that certain salt cations promote hydrophobic interactions between a virus and a filter or substrate. The cations that are most effective are smaller, monovalent or multivalent ions (6, 12). These salt cations also interfere with the electrostatic interactions that might occur between a virus and a filter. This is probably a result of screening of charges by ions in solution (5) and has been observed in other studies (15, 20, 21). Electrostatic interactions influence viral adsorption in many cases. Such situations include situations in which a filter surface is electropositive and the pH value of the solution is near or greater than the virus isoelectric point (19, 24). Electrostatic interactions also are important when the filter surface is electronegative and the pH value of the solution is below the virus isoelectric point (2, 3, 8, 18). The presence of both urea and a multivalent salt is sufficient to overcome most of the forces responsible for viral adsorption to solid surfaces. The type of salt appears to be more important than the ionic strength of the salt in promoting adsorption to Millipore filters for some viruses (MS2 and PRD-1) but not for others (X174 and poliovirus 1).
Both the ionic strength and the type of salt appear to influence virus
adsorption to 1MDS filters. Solutions of sodium chloride, magnesium
chloride, and aluminum chloride having the same ionic strength all
interfered with virus adsorption, but solutions of aluminum chloride
resulted in the most interference.
In summary, the results of this study show that salts can promote virus
adsorption, interfere with virus adsorption, or have little effect on
virus adsorption. Virus adsorption to solids is the result of many
interactions; therefore, theories on the effects of salts on virus
adsorption should account for the multiple effects observed.
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ACKNOWLEDGMENTS |
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We acknowledge the financial contribution of the Engineering Research Center (ERC) for Particle Science and Technology at the University of Florida, National Science Foundation grant EEC-94-02989, and the Industrial Partners of the ERC.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Microbiology and Cell Science, University of Florida, Gainesville, FL 32611-0700. Phone: (352) 392-1885. Fax: (352) 392-5922. E-mail: george{at}micro.ifas.ufl.edu.
Paper number R-07534 from the Florida Agricultural Experiment
Station, Gainesville.
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REFERENCES |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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| 1. | Ackermann, H. W., and S. D. Michael. 1987. Viruses of procaryotes, p. 173-201. CRC Press, Boca Raton, Fla. |
| 2. | American Public Health Association. 1998. Standard methods for the examination of water and wastewater, p. 9:117-9:119. American Public Health Association, New York, N.Y. |
| 3. | Berg, G., R. S. Safferman, D. R. Dahling, and D. Berman. 1984. U. S. EPA manual of methods for virology. Publication EPA-600/4-84-013. Environmental and Support Laboratory, Cincinnati, Ohio. |
| 4. | Bitton, G. 1980. Adsorption of viruses to surfaces: technological and ecological implications., p. 332-374. In G. Bitton, and K. C. Marshall (ed.), Adsorption of microorganisms to surfaces. John Wiley & Sons, New York, N.Y. |
| 5. | Cantor, C. R., and P. R. Schimmel. 1980. Biophysical chemistry, p. 676-678. W. H. Freeman and Company, San Francisco, Calif. |
| 6. |
Farrah, S. R.
1982.
Chemical factors influencing adsorption of bacteriophage MS2 to membrane filters.
Appl. Environ. Microbiol.
43:659-663 |
| 7. |
Farrah, S. R., and G. Bitton.
1978.
Elution of poliovirus adsorbed to membrane filters.
Appl. Environ. Microbiol.
36:982-984 |
| 8. |
Farrah, S. R.,
C. P. Gerba,
C. Wallis, and J. L. Melnick.
1976.
Concentration of viruses from large volumes of tap water using pleated membrane filters.
Appl. Environ. Microbiol.
31:221-226 |
| 9. | Farrah, S. R., S. M. Goyal, C. P. Gerba, C. Wallis, and J. L. Melnick. 1978. Concentration of poliovirus from tap water onto membrane filters with filters with aluminum chloride at ambient pH levels. Appl. Environ. Microbiol. 36:624-626. |
| 10. | Farrah, S. R., S. M. Goyal, C. P. Gerba, C. Wallis, and P. T. B. Shaffer. 1976. Characteristics of humic acid and organic compounds concentrated from tap water using the Aquella virus concentrator. Water Res. 10:897-901[CrossRef]. |
| 11. |
Farrah, S. R., and D. R. Preston.
1985.
Concentration of viruses from water by using cellulose filters modified by in situ precipitation of ferric and aluminum hydroxide.
Appl. Environ. Microbiol.
50:1502-1504 |
| 12. |
Farrah, S. R.,
D. O. Shah, and L. O. Ingram.
1981.
Effects of chaotropic and antichaotropic agents on elution of poliovirus adsorbed on membrane filters.
Proc. Natl. Acad. Sci. USA
78:1229-1232 |
| 13. | Gerba, C. P. 1984. Applied and theoretical aspects of virus adsorption to surfaces. Adv. Appl. Microbiol. 30:133-168[Medline]. |
| 14. | Kessick, M. A., and R. A. Wagner. 1978. Electrophoretic mobilities of virus adsorbing filter materials. Water Res. 12:263-268[CrossRef]. |
| 15. |
Lytle, C. D.,
L. B. Routson,
N. B. Jain,
M. R. Myers, and B. L. Green.
1999.
Virus passage through track-etch membranes modified by salinity and a nonionic surfacant.
Appl. Environ. Microbiol.
65:2773-2775 |
| 16. | Mix, T. W. 1974. The physical chemistry of membrane-virus interaction. Dev. Ind. Microbiol. 15:136-142. |
| 17. | Mix, T. W. 1987. Mechanism of adsorption and elution of viruses to and from surfaces, p. 127-137. In G. Berg (ed.), Methods for recovering viruses from the environment. CRC Press, Boca Raton, Fla. |
| 18. | Payment, P., C. P. Gerba, C. Wallis, and J. L. Melnick. 1976. Methods for concentrating viruses from large volumes of estuarine water on pleated membrane filters. Water Res. 10:893-896[CrossRef]. |
| 19. |
Preston, D. R.,
T. V. Vasudevan,
G. Bitton,
S. R. Farrah, and J.-L. Morel.
1988.
Novel approach for modifying microporous filters for virus concentration from water.
Appl. Environ. Microbiol.
54:1325-1329 |
| 20. |
Shields, P. A., and S. R. Farrah.
1983.
Influence of salts on electrostatic interactions between poliovirus and membrane filters.
Appl. Environ. Microbiol.
45:526-531 |
| 21. | Shields, P. A., T. F. Ling, V. Tjatha, D. O. Shah, and S. R. Farrah. 1986. Comparison of positively charged membrane filters and their use in concentrating bacteriophages in water. Water Res. 20:145-151. |
| 22. | Smith, E. M., and C. P. Gerba. 1982. Laboratory methods for the growth and detection of animal viruses, p. 15-47. In C. P. Gerba, and S. M. Goyal (ed.), Methods in environmental virology. Marcel Dekker, Inc., New York, N.Y. |
| 23. | Snustad, S. A., and D. S. Dean. 1971. Genetic experiments with bacterial viruses. W. H. Freeman and Co., San Francisco, Calif. |
| 24. |
Sobsey, M. D., and J. S. Glass.
1980.
Poliovirus concentration from tap water with electropositive adsorbent filters.
Appl. Environ. Microbiol.
40:201-210 |
| 25. |
Sobsey, M. D., and J. S. Glass.
1984.
Influence of water quality on enteric virus concentration by microporous filter methods.
Appl. Environ. Microbiol.
47:956-960 |
| 26. | Stana-Kleinschek, K., and V. Ribitsch. 1998. Electrokinetic properties of processed cellulose fiber. Colloids Surf. A Physiochem. Eng. Aspects 140:127-138[CrossRef]. |
| 27. | Wallis, C., M. Henderson, and J. L. Melnick. 1972. Enterovirus concentration on cellulose membranes. Appl. Microbiol. 23:476-480[Medline]. |
| 28. | Wallis, C., J. L. Melnick, and C. P. Gerba. 1979. Concentration of viruses from water by membrane chromatography. Annu. Rev. Microbiol. 33:413-437[CrossRef][Medline]. |
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