Environmental Technology

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Water treatment with exceptional virus

inactivation using activated carbon modified with
silver (Ag) and copper oxide (CuO) nanoparticles

Quelen Letícia Shimabuku, Flávia Sayuri Arakawa, Marcela Fernandes Silva,

Priscila Ferri Coldebella, Tânia Ueda-Nakamura, Márcia Regina Fagundes-
Klen & Rosangela Bergamasco

To cite this article: Quelen Letícia Shimabuku, Flávia Sayuri Arakawa, Marcela Fernandes Silva,
Priscila Ferri Coldebella, Tânia Ueda-Nakamura, Márcia Regina Fagundes-Klen & Rosangela
Bergamasco (2016): Water treatment with exceptional virus inactivation using activated carbon
modified with silver (Ag) and copper oxide (CuO) nanoparticles, Environmental Technology

To link to this article: http://dx.doi.org/10.1080/09593330.2016.1245361

Published online: 21 Oct 2016.

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ENVIRONMENTAL TECHNOLOGY, 2016
http://dx.doi.org/10.1080/09593330.2016.1245361

Water treatment with exceptional virus inactivation using activated carbon

modified with silver (Ag) and copper oxide (CuO) nanoparticles
Quelen Letícia Shimabukua,b, Flávia Sayuri Arakawa a, Marcela Fernandes Silvaa, Priscila Ferri Coldebellaa,
Tânia Ueda-Nakamura c, Márcia Regina Fagundes-Klenb and Rosangela Bergamascoa
a
Department of Chemical Engineering, State University of Maringá, Maringá, Paraná, Brazil; bDepartment of Chemical Engineering, University of
West Parana, Toledo, Paraná, Brazil; cDepartment of Basic Health Sciences, State University of Maringá, Maringá, Paraná, Brazil

ABSTRACT ARTICLE HISTORY

Continuous flow experiments (450 mL min−1) were performed in household filter in order to Received 4 April 2016
investigate the removal and/or inactivation of T4 bacteriophage, using granular activated carbon Accepted 2 October 2016
(GAC) modified with silver and/or copper oxide nanoparticles at different concentrations. GAC
KEYWORDS
and modified GAC were characterized by X-ray diffractometry, specific surface area, pore size Activated carbon; silver;
and volume, pore average diameter, scanning electron microscopy, transmission electron copper oxide; nanoparticle;
microscopy, zeta potential and atomic absorption spectroscopy. The antiviral activity of the characterization; viral
produced porous media was evaluated by passing suspensions of T4 bacteriophage inactivation
(∼105 UFP/mL) through filters. The filtered water was analyzed for the presence of the
bacteriophage and the release of silver and copper oxide. The porous media containing silver
and copper oxide nanoparticles showed high inactivation capacity, even reaching reductions
higher than 3 log. GAC6 (GAC/Ag0.5%Cu1.0%) was effective in the bacteriophage inactivation,
reaching 5.53 log reduction. The levels of silver and copper released in filtered water were below
the recommended limits (100 ppb for silver and 1000 ppb for copper) in drinking water. From
this study, it is possible to conclude that activated carbon modified with silver and copper oxide
nanoparticles can be used as a filter for virus removal in the treatment of drinking water.

[15]. In addition, conventional treatment methods such

1. Introduction
Drinking water in large amounts and with good quality is
currently and for the next decades an increasingly great
concern. Among the factors that contribute to this crisis
are population growth and urbanization, deterioration of
water treatment and supply infrastructures, increasing
influence of residual waters and biosolids in drinking
water sources and the growing number of emergent
contaminants still difficult to be identified [1].
With the advancement of detection techniques based
on molecular biology, it turned out to be possible to
detect genome fragments of viral genomes in the
environment including drinking water sources, thus point-
ing out the necessity of guaranteeing the removal of
viruses and other pathogens in water treatment plants
in order to maintain society’s health and welfare [2,3].
These viral and bacterial pathogens present in water
represent a great risk for human health and may cause
diseases such as diarrhea, acute gastroenteritis, conjunc-
tivitis and respiratory diseases [4–14]. The removal of
pathogenic viruses from water becomes a technological
challenge due to their small dimensions (20–250 nm)
as chlorination are ineffective at inactivating viruses
[16,17].
Experimental difficulties with enteric viruses are widely
known, detection techniques are expensive, long-lasting
and hard to work with, but they can be avoided, provided
that they are simulated by bacteriophages such as MS2,
phi X-174 and T4, also known as indicator microorganisms
[18,19]. The similar behavioral characteristics of both
viruses and bachteriophages in porous media were
reported by Grabow [20] and are the most common
analytical tools for the study of viruses [21–24].
MS2 and T4 bacteriophages are categorized as being
representatives of adsorption behavior in solids (empiri-
cally analyzed in different particles) concerning the two
main categories of human viruses in the study described
by Gerba [25]. In this way, using both phages as viral sub-
stitutes, an adsorption behavior of a wide array of human
viruses can be foreseen [26].
One of the most utilized adsorbents worldwide is acti-
vated carbon, due to its nanostructure, high porosity,
large specific surface, distribution of pore size and struc-
ture [27–29] and it is widely used in organic effluents’

CONTACT Rosangela Bergamasco rbergamasco@uem.br Department of Chemical Engineering, State University of Maringá, Avenida Colombo, 5790.
Bloco D90, 87020–900, Maringá, Paraná, Brazil
© 2016 Informa UK Limited, trading as Taylor & Francis Group
2 Q. L. SHIMABUKU ET AL.

treatment [30–33]. Activated carbon, however, does not
present relevant capacity to remove microorganisms
that might be present in water. According to Hijnen
et al. [34], granular activated carbon (GAC) in adsorption
filters does not present virus removal in water treatment.
Notwithstanding, a structure modification, such as the
introduction of biocide materials, can improve its micro-
organism removal capacity [35].
Modifications in order to potentiate existing antiviral
components and develop new antiviral agents constitute
research priority [36]. Several approaches to the possi-
bility of modifying the filtering medium in order to
improve both its microorganism removal capacity and
water quality are presented in the literature: granular
anthracite and GAC coated with nanoporous Al2O3 [37]
and layered double hydroxide nanocomposites [38],
nanostructured surface modification of microporous cer-
amics [15], microporous ceramics modified with yttrium
oxide [39], glass fiber-coated with hematite nanoparti-
cles [23], nanofilter from carbon nanotubes [40],
iron-oxide-amended biosand filters [41], biosand filter
modified with iron-oxide-coated sand [42], zero-valent
iron [1] and super-powdered activated carbon [2].
More recently, GAC and other adsorbent media were
impregnated with metal compounds such as silver [3,36]
and copper [43,44] in order to increase the removal effi-
ciency of contaminants. Nanotechnology provides prom-
ising possibilities for the impregnation of these metal
compounds through the modification of metals/metal
compound characteristics in order to improve their phys-
ical–chemical and biological properties [45]. Nanoparti-
cles and silver ions presented antimicrobial properties
[46–48], thus helping/promoting viral and bacterial inac-
tivation [3,36].
The only disadvantage presented by silver is its high
cost, since silver salts precursors necessary to the obtain-
ment of silver metal usually present value a little above
average. As a low-cost alternative to silver nanoparticles,
the use of copper nanoparticles has been investigated in
water purification filters [43]. Copper presents lower cost
when compared with silver and it is very effective in the
elimination of pathogenic agents such as viruses and
bacteria [49,50]. Thus, copper nanoparticles present
potential application as antimicrobial agents in water
purification and can be incorporated in fibrous materials
to act as support of copper ions in order to enhance anti-
microbial activity [51,52].
the necessity of developing and testing filtering media (fil-
tration/adsorption) to use in household water filters, thus
obtaining highly effective virucidal materials or products
in order to prevent virus transmission or eliminate infec-
tion sources in the environment [49].
By combining the adsorbent properties of activated
carbon with the diverse properties of silver and copper
nanoparticles it was possible to evaluate the removal/
inactivation capacity of T4 bacteriophages obtained
with the use of compounds of the different metals
studied and the synergistic effect among them. The
aim of this study is to modify, characterize and evaluate
the use of GAC coated with silver and copper for virus
removal. In this study the removal/inactivation of T4 bac-
teriophage by GAC modified with metal compounds of
silver and copper is reported.
2. Materials and methods
2.1. Materials
GAC of oil palm shells, made by Bahiacarbon (Bahia,
Brazil), was utilized in this study as a matrix for impreg-
nation and its surface area of 575 m2 g−1. As for the
modification of activated carbon surface by silver and
copper impregnation, AgNO3 analytic grade (Nuclear
Company) and CuSO4 (II) analytic grade (Vetec Ltda)
were used, respectively.
The contaminated water used in the experiments was
prepared from a solution of T4 bacteriophage
(109 UFP mL−1) diluted in distilled water until reaching
a concentration of approximately 105 UFP mL−1 [26,54].
All the materials used were heated in an autoclave at
121°C for 15 min before being used.
2.2. Modification/Impregnation of activated
carbon
GAC was modified by silver and/or copper impregnation
at different metal concentrations in a w/w (%) in relation
to the activated carbon. The nominal concentrations
used are shown in Table 1.
Table 1. Nominal concentrations of metals silver and copper
impregnated on the surface of GAC.
Nominal
concentration
w/w (%)
Sample Ag Cu Nomenclature

The lack of drinking water in a multitude of places GAC/Ag0.5% 0.5 – GAC1

GAC/Ag1.0% 1.0 – GAC2
throughout the world is a significant concern for human GAC/Cu0.5% – 0.5 GAC3
health. Household filters for water purification offer an GAC/Cu1.0% – 1.0 GAC4
GAC/Ag0.5%Cu0.5% 0.5 0.5 GAC5
accessible and convenient form of reducing the expo- GAC/Ag0.5%Cu1.0% 0.5 1.0 GAC6
sition to pathogenic microorganisms [53] wherever GAC/Ag1.0%Cu0.5% 1.0 0.5 GAC7
GAC/Ag1.0%Cu1.0% 1.0 1.0 GAC8
water supply problems might occur. There is, however,

GAC was impregnated using an incipient wetness
impregnation method. The GAC was placed in the flask
of the rotary evaporator and deionized water was
added in a 1:1 proportion, consisting of 200 g of acti-
vated carbon in 200 mL of water. Subsequently, AgNO3
and/or CuSO4 (II) salt was dissolved in 30 mL of deionized
water and the solution was placed in the flask. This
mixture was kept under rotation of 20 rpm at 60°C for
24 h. The excess water was vacuum-extracted and the
sample was dried in an oven at 100°C for 24 h. A heat
treatment was applied at 350°C in a resistive oven for
7 h to enhance the impregnation of the metal in the
carbon surface and eliminate anions of metal salts that
occupy the adsorption sites, which are supposed to be
free [55].
2.3. Characterization of GAC and modified GAC
GAC and modified GAC were characterized by X-ray
diffractometry, using the nitrogen adsorption/desorption
method to obtain specific surface area (SBET), t micro-
pores’ area (Smic t), pores’ average diameter (dp), pores’
total volume (Vt) and micropores’ volume (Vmic), scan-
ning electron microscopy (SEM), transmission electron
microscopy (TEM), zeta potential and atomic absorption
spectroscopy. X-ray diffraction (XRD), a technique which
reveals detailed and precise microstructures, was used
to identify metal compounds produced and estimate
the size of the particles. Wide-angle XRD and patterns
of samples were obtained with a diffractometer (Bruker-
AXS D8 Advance), for 2θ values ranging from diffraction
angles between 20° and 85° and equipped with a rotation
anode using CuKα radiation (λ = 0.15418 nm).
Evaluations for BET (Brunauer–Emmett–Teller)-
specific surface area and pore volume and size were
determined by a nitrogen gas adsorption analyzer
using Autosorb Nova 1200 Series (Quantachrome Instru-
ments) The nitrogen adsorption–desorption data were
recorded for N2 liquid at 77 K. A Shimadzu scanning elec-
tron microscope (SEM) model SS550 Superscan was used
to analyze the morphology of the samples coated by
gold sputtering.
TEM measurements were performed on a JEOL JEM-
1400 with 120 kV. The samples were deposited on a
pure carbon thin film Cu grid (with 200 mesh) (CF200-
Cu, EMS). Samples were prepared for TEM analysis by
sonicating them for 2 min and then depositing the
metal nanoparticles on the TEM lacy copper support
grids for samples’ dispersion. The grids were allowed
to dry before being mounted on the TEM sample holder.
The zeta potentials of the materials were examined on
the Beckman-Colter Delsa NanoTM Zeta Potential
ENVIRONMENTAL TECHNOLOGY 3
(Beckman Coulter) that uses electrophoretic light scatter-
ing for zeta potential determination.
In order to verify silver and copper concentrations in
the filtered water, it was adopted the sample digestion
methodology in agreement with nitric acid digestion
for flame atomic absorption and high-level concen-
trations – 3030E – standard methods [56]. Silver and
copper concentrations were analyzed by flame atomic
absorption spectroscopy, using SpetraAA 50 B Varian
Atomic Absorption Spectrometer equipment.
2.4. Culture and analysis of T4 bacteriophage
T4 Bacteriophage (ATCC) was selected as a model virus
because of its structural similarity with most enteric
human viruses and also its easy use. T4 is a tailed
phage of the Myoviridae family with linear double-
stranded DNA, whose overall size is 90 nm wide by
200 nm long [18,24,26].
The T4 Bacteriophage was replicated and purified as
described by Russel et al. [57]. In a summarized way,
Escherichia coli, used host cells, were cultivated in
triptic soy broth solution and, subsequently, inoculated
with T4. T4 was purified by centrifugation at 2000 rpm
for 10 min and at the temperature of −4°C, in order to
remove residues. The final T4 stock was stored at 4°C
and a concentration of approximately 109 UFP mL−1.
Quantification of T4 bacteriophage was carried out
according to the double layer agar procedure (upper
layer of 0.7% TSA, lower layer of 1.5% TSA) [3,41,58,59].
Briefly, plaques formed due to the inoculation of E. coli
with T4 at 37°C for 24 h, and plates with between 30
and 300 plaques were used for calculating the concen-
tration of T4. Any plates containing more than 300
plaques were quantified from a higher dilution plate.
Virus efficiency removal was expressed by a log
reduction value (LRV). This value is defined by LRV =
log (Cf/Cp), in which Cf and Cp represent virus feed and
permeate concentrations, respectively. When no virus is
detected in the permeate, Cp is lower than 1 UFP mL−1
and LRV can be reported as being higher than log of Cf
[40].
All the materials that had any contact with the virus
solution, filtering medium and reagents were sterilized
in autoclave or purchased as sterile.
2.5. Virus removal by filtration
Continuous flow filtration experiments were carried out
in order to test the removal/inactivation capacity of T4
in GAC-GAC8. The filter was preconditioned with 3 L of
distilled water. Phage particles were added in distilled
water and homogenized at 100 rpm for 3 min followed
4 Q. L. SHIMABUKU ET AL.
by 20 min of mixing at 30 rpm, using a Jar Test device
[26]. The aim of this process was to create a concentrated
homogeneous solution of particles which might be
added to the produced filters. The solution containing
virus was continuously pumped by means of a peristaltic
pump at a constant flow of approximately 450 mL min−1,
through the filtering medium, placed in a column of
7.5 cm diameter and 8.5 cm high, with a volume of
375.33 cm3. Each column was filled with 150 g of the
material to be tested (GAC-GAC8). For each test, 10 L of
viral solution [54,60] with approximate concentration of
105 UFP mL−1 [26,54] and pH 7 was utilized. The exit
sample (10 mL) was collected at the end of the filtered
volume (10 L) and the viruses were quantified in order
to determine filter efficiency. The tests were carried out
in triplicate so as to ensure results’ reproducibility.
Average values and standard deviations were deter-
mined in order to represent each evaluation.
For the virus filter that showed higher removal effi-
ciency, it was an evaluated lifetime with viral solution
with an approximate concentration of 105 UFP mL−1 for
determining the saturation point of the sample.
2.6. Statistical analysis
In order to evaluate virus removal efficiency by the pre-
pared activated carbons, a 32 factorial experimental deli-
neation, with two impregnation metals (Ag and Cu) and
3 concentration levels of impregnation metals (0.0%,
0.5% and 1.0%) was used. The verification of statistical
differences between the activated carbons was deter-
mined by means of viral removal efficiency, with the
use of ANOVA variance analysis and comparison of the
means by the Tukey test, at 5% significance level, that
is, by considering significant values at a p-value < 0.05.
The software used for statistical analysis was Statistic 8.0.
3. Results and discussions
3.1. Characterization of pure and modified GAC
According to the X-ray diffractograms, in Figure 1, the
observed peaks correspond to diffraction patterns of
Ag in the form Ag0, and Cu in the form CuO and Cu2O.
The obtainment of copper oxides instead of metallic
copper is due to the ambient atmosphere used in the
synthesis. These results are in agreement with the ones
obtained by Huang et al. [61] and Siriwardane et al. [62].
In Figure 1, Ag0 peaks were identified in samples
of GAC1, GAC2, GAC5, GAC 6, GAC7 and GAC8, at 2θ
= 38.1° (111), 44.5° (200), 64.5° (220) and 77.6° (311)
[61–64]. The main structures of activated carbon are
amorphous and present broad reflections in the range
of 2θ = 10–30° [28], whose structure does not possess a
spatial ordering at long distance.
The incorporation of copper in the form of copper
oxide on the surface of GAC became evident in the dif-
fractograms (Figure 1), by observing peaks of cupric
oxide and cuprous oxide in the sample GAC3, GAC4,
GAC5, GAC6, GAC7 and GAC8. At 2θ = 39° (200) CuO
was identified [50] and at 2θ = 36.4° (111) and 42.3
(200) Cu2O was identified [43,65].
For all the samples of activated carbon modified with
silver and/or copper it is possible to identify peaks of
metallic silver, cupric and/or cuprous oxides and the crys-
talline forms found can be justified by the temperature
used in the calcination process, 350°C. According to Sir-
iwardane et al. [62] degradation temperature of copper
sulfate to copper metal is in the range 600–700°C and,
according to Huang et al. [61], degradation temperature
of silver nitrate to silver metal is around 350°C. Since the
temperature used in the impregnation process reached
up to 350°C, the presence of silver metal and copper
oxides is accounted for.
The average diameters of produced Ag and CuO par-
ticles were also estimated (Table 2), by using (111) peak
for silver particles and (111) for CuO particles at 2θ 38.1°
and 36.4°, respectively, in which a Lorentzian curve was
fitted for the determination of full width at half-
maximum (FWHM) and obtainment of diameters by
Scherrer Equation, d = 0.9l/bcos u.
Where d is the average diameter of the crystals, λ
(0.154 nm) is the X-ray wavelength, β (radians) is the
line broadening from the FWHM of the peak and θ is
the Bragg angle. Particle sizes in the range from 25 to
Figure 1. X-ray diffractograms of the samples GAC (non-modified
activated carbon) GAC1 (GAC/Ag0.5%), GAC2 (GAC/Ag1.0%),
GAC3 (GAC/Cu0.5%), GAC4 (GAC/Cu1.0%), GAC5 (GAC/Ag0.5%
Cu0.5%), GAC6 (GAC/Ag0.5%Cu1.0%), GAC7 (GAC/Ag1.0%
Cu0.5%), GAC8 (GAC/Ag1.0%Cu1.0%) where *Ag0 and 0CuO/
0Cu2O.
 ENVIRONMENTAL TECHNOLOGY 5

Table 2. Average diameter of Ag and CuO crystallites of modified is type I, in which microporous adsorption is the promi-
samples estimated by the Scherrer Equation. nent adsorption [68]. The adsorbed volume stabilized
Sample Average crystallite diameter (nm) when relative pressure was higher than 0.2.
Ag CuO Considering the importance of surface area of the
GAC1 34 – materials for adsorption applications, and also taking
GAC2 37 –
GAC3 – 22 into account the impregnation of nanoparticles in
GAC4 – 35 carbon, it was possible to evaluate the modifications
GAC5 25 32
GAC6 40 34 caused by the impregnation process in the character-
GAC7 35 32 istics of the samples. In Table 3, the values of surface
GAC8 33 37
area and porosity of GAC-GAC8 are shown. GAC utilized
in the present work presents a BET surface area of
40 nm were found for silver nanoparticles and from 22 to 575 m2 g−1, with average pore diameter of 1.19 nm.
37 nm for copper oxide nanoparticles. Earlier works also Average pore diameters of the samples after impreg-
observed particle sizes in the range 5–30 nm [36] and nation lay between 1.16 and 1.18 nm, confirming the
30–80 nm [66] for silver nanoparticles and from 20 to microporous characteristic of the material.
27 nm [67] for copper oxide nanoparticles. After the incorporation of silver and/or copper oxide
Adsorption/desorption isotherms of GAC-GAC8, pre- on the surface of GAC, BET surface area decreased to
sented in Figure 2, were obtained in order to assess values between 508 and 567 m2 g−1. These values were
the influence of nanoparticles’ impregnation in the coherent with values found for commercial activated
surface area of carbon. It can be seen that, for GAC and carbon and activated carbon modified with metals, as
modified GAC, the adsorbed volume increased rapidly reported by Srinivasan et al. [64], Lam and Hu [65], Para-
with the increase of pressure in low pressure ranges, shar et al. [66] and Freitas et al. [69]. There was a decrease
which means that the adsorption/desorption isotherm in the parameters’ micropores’ area (t method), pores’

Figure 2. N2 adsorption/desorption isotherms of activated carbon samples (a) GAC (non-modified activated carbon), GAC1
(GAC/Ag0.5%), GAC2 (GAC/Ag1.0%); (b) GAC3 (GAC/Cu0.5%), GAC4 (GAC/Cu1.0%); and (c) GAC5 (GAC/Ag0.5%Cu0.5%), GAC6
(GAC/Ag0.5%Cu1.0%), GAC7 (GAC/Ag1.0%Cu0.5%), GAC8 (GAC/Ag1.0%Cu1,0%).
6 Q. L. SHIMABUKU ET AL.

Table 3. Values of surface area and porosity of GAC and modified of various sizes on the surface of activated carbon. The
GAC samples. structures of GAC1, GAC4 and GAC6 are similar to that
Amostra SBET (m2/g) Smic t (m2/g) Dp (nm) Vt (cm3/g) Vmic (cm3/g) of commercial GAC, thus showing that the incorporation
GAC 575 456 1.19 0.343 0.302 of silver and/or copper oxide did not change the surface
GAC1 497 374 1.16 0.286 0.268
GAC2 567 409 1.16 0.328 0.295 morphology of GAC. GAC2, GAC3, GAC4, GAC5, GAC7
GAC3 511 401 1.16 0.326 0.308 and GAC8 samples presented micrographs not showed
GAC4 566 416 1.18 0.335 0.295
GAC5 539 403 1.16 0.338 0.319 similar to the ones shown in Figure 3.
GAC6 543 422 1.16 0.316 0.291 TEM images of the samples GAC, GAC1, GAC4 and
GAC7 528 412 1.18 0.341 0.319
GAC8 508 418 1.18 0.321 0.318
GAC6 are shown in Figure 4. Size, morphology and
nanostructures of the samples were observed by using
TEM. Due to contrast difference, silver and copper
average diameter, pores’ total volume and micropores’ oxide nanoparticles can be seen as superposed dark
volume when compared with GAC, suggesting total dots on the surface of GAC [64,71].
and/or partial blockage/incorporation of some pores by In the GAC sample only the morphology of activated
silver and/or copper oxide deposition through the carbon is observed, as expected. TEM micrographs of
impregnation process [28,61,70], with the possibility of activated carbon samples containing Ag and CuO/Cu2O
occurring either externally or internally to the pores nanoparticles presented an average diameter lower
[65]. The incorporation of silver and copper oxide on than 50 nm, in agreement with the results obtained by
the surface of activated carbon did not alter the micro- XRD and shown in Table 2. GAC2, GAC3, GAC4, GAC5,
porous characteristic of the porous media produced. GAC7 and GAC8 samples presented micrographs
GAC, GAC1, GAC4 and GAC6 surface morphologies are similar to the ones shown in Figure 4.
presented in the micrographs (SEM) in Figure 3. As can For a better understanding of the obtained results,
be seen (Figure 3), GAC has a porous and irregular struc- measurements of zeta potential of GAC-GAC8 samples
ture, indicating a smooth surface with dispersed cavities and T4 bacteriophage were carried out so as to verify

Figure 3. SEM micrographs of the samples (a) GAC (non-modified activated carbon), (b) GAC1 (GAC/Ag0.5%), (c) GAC4 (GAC/Cu1.0%)
and (d) GAC6 (GAC/Ag0.5%Cu1.0%).
 ENVIRONMENTAL TECHNOLOGY 7

Figure 4. TEM micrographs of the samples (a) GAC (non-modified activated carbon), (b) GAC1 (GAC/Ag0.5%), (c) GAC4 (GAC/Cu1.0%)
and (d) GACG6 (GAC/Ag0.5%Cu1.0%).

whether the surface charge presented by the samples Bacteriophage) present negative surface charges. Then,
would generate attractive or repulsive forces in the com- it is possible to infer that between the adsorbent and
bination of GAC-GAC8/T4 bacteriophage. These results adsorbate occur van der Waals repulsive electrostatic
are presented in Table 4. sum and retarded forces (interactions) [23,72,73].
Considering the results presented for the studied
samples in Table 4, it can be observed that both the
adsorbent material (GAC-GAC8) and the adsorbate (T4
3.2. Virus removal/inactivation
Removal efficiency of T4 bacteriophage was assessed in
Table 4. Zeta potential values of the samples GAC-GAC8 and T4
the filters produced with GAC-GAC8. Reductions of
bacteriophage, obtained at pH 7, in 0.3 mMol of NaCl solution.
Sample Zeta potential (mV)
log10 obtained by means of continuous flow of the con-
GAC −24.54 (±0.25)
taminated solution through GAC-GAC8 and the statistical
GAC1 −40.87 (±0.67) analysis of inactivation efficiency of the filters are shown
GAC2 −37.39 (±1.07) in Figure 5.
GAC3 −33.97 (±3.32)
GAC4 −33.84 (±0.89) For GAC filter, viral reduction was 0.32 log. This low
GAC5 −31.15 (±2.61) reduction value was also reported by Hijnen et al. [34],
GAC6 −32.25 (±1.39)
GAC7 −35.62 (±0.96) who, in their study, showed that GAC filters do not
GAC8 −36.79 (±0.52) present efficiency in the elimination of virus in water
Bacteriophage T4 −41.94 (±0.92)
treatment. Other authors also reported low capacity of
8 Q. L. SHIMABUKU ET AL.
Figure 5. T4 bacteriophage inactivation in filtration experiments
with the samples of GAC (non-modified activated carbon, GAC1
(GAC/Ag0.5%), GAC2 (GAC/Ag1.0%), GAC3 (GAC/Cu0.5%), GAC4
(GAC/Cu1.0%), GAC5 (GAC/Ag0.5%Cu0.5%), GAC6 (GAC/Ag0.5%
Cu1.0%), GAC7 (GAC/Ag1.0%Cu0.5%) and GAC8 (GAC/Ag1.0%
Cu1.0%). Values expressed by the average. Average values fol-
lowed by the same letter do not statistically differ from one
another, using the Tukey test at 5% significance level.
filtration in GAC when it comes to viral and bacterio-
phages’ removal (0.2–0.7 log) [74–76]. Since the pores
of the filtering medium are, at least, one order of magni-
tude lower than the tested particles (T4 bacteriophage),
physical retention may occur.
Despite the negative zeta potential presented by T4
particles and the porous medium (Table 4), Cookson Jr
[77] suggests that T4 adsorption may occur due to elec-
trostatic attraction between the carboxyl groups in the
activated carbon and amino groups on the virus
surface. However, the low removal value for GAC can
also be ascribed to the fact that both present negative
surface charge, which prevents particles from approach-
ing the filtering medium close enough to cause Van der
Waals attractive forces to prevail, thus causing a reten-
tion drop [39,59].
The effect of different concentrations of silver and
copper oxide used to modify the GAC, concerning virus
inactivation, are also shown in Figure 5. For samples con-
taining only copper oxides (CuO and Cu2O) in 0.5% and
1% concentrations (GAC3 and GAC4) viral inactivation
did not present significant statistical difference (p-value
< .05) when compared with non-modified GAC, which
presented 0.33 log reduction, indicating that the presence
of copper oxide nanoparticles, at both concentrations
studied, on the carbon surface, was not efficient to
improve inactivation in GAC. GAC1 and GAC2 presented
an increase in efficiency, 0.45 log of inactivation and
0.64 log of inactivation, respectively. These filters demon-
strated significant statistical difference when compared
with GAC. As a result, it is possible to assume that the pres-
ence of Ag at 0.5% and 1% concentrations is efficient at
improving virus inactivation when compared with GAC.
However, there was no significant statistical difference
between GAC1 and GAC2 filters, that is, the use of silver
concentration of 0.5% and 1% does not differ statistically
from one another.
For the filters in which silver and copper oxide mix-
tures were used in different concentrations (GAC5,
GAC6, GAC7 and GAC8), viral reduction reached values
higher than 3.02 log of inactivation (Figure 5). This
demonstrates that the simultaneous presence of silver
and copper oxides in the samples enhances significantly
viral inactivation efficiency. For the filters GAC6, GAC7
and GAC8 viral reductions were higher than 5 log. The
statistical analysis demonstrated that there is no signifi-
cant statistical difference among these filters, that is,
silver and copper oxide concentrations utilized in this
study caused the same viral reduction effect, meaning
that the one with the lower silver concentration (GAC6)
is the most advantageous, due to the high cost of this
metal.
The combination of silver and copper oxides utilized
in GAC modification presented a synergistic effect con-
cerning virus inactivation. These same concentrations,
when used separately, showed lower efficiencies.
Inactivation enhancement of the bacteriophage by
adsorbent media modified with silver can be explained
as a result of the interactions of carboxyl groups in the
amino acids of proteins on the virus surface with silver
[3,23,78]. Most viruses have surfaces compounded of
polypeptides from protein that contains amino acids,
such as glutamic acid, aspartic acid, histidine and tyro-
sine [25]. The easy formation of insoluble compounds
with anions, sulfhydryl groups and many biological
materials, such as enzymes, is also responsible for the
disinfecting activity of silver [79].
Auffan et al. [80] suggest that the most important par-
ameter to control cytotoxicity of metal nanoparticles is
their chemical stability, since it is related to the dissol-
ution of metal nanoparticles as well as to catalytic prop-
erties and modifications of the redox surface. The release
of Ag+ ions from silver nanoparticles is very often
accompanied by the generation of reactive oxygen
species (ROS) [81] also involving interaction with viral
DNA and thiol groups from proteins [82]. Thus, the
observed toxicity may be induced by released ions,
ROS or both [83]. Lund [84] concluded that the inacti-
vation capacity of heavy metal ions is due to their oxidiz-
ing power and also suggested that there is a functional
relationship between the inactivation rate and the oxi-
dation potential of the ions. Inactivation may have
targets such as proteins or nucleic acids.

On the other hand, the significant antiviral property of
copper nanoparticles has been ascribed to the release of
Cu+, followed by the generation of ROS, such as the
hydroxyl radical, and subsequent oxidation of amino
acids from the proteins of the virus capsid [85]. Yama-
moto et al. [86] observed that inactivation due to
copper is related to traces of electrolytically formed
hydrogen peroxide. Copper nanoparticles can be pro-
posed as useful sources of a continuous supply of Cu+
ions and be responsible for the toxic action of copper
ions in virus inactivation. Copper possesses high affinity
with sulfhydryl groups [79]. Murray and Laband [87] indi-
cated that not only had the virus been inactivated by
CuO surface but also virus degradation had occurred,
because analyses of elluated viruses indicated that the
proteins were divided into small fragments. Metal and
metal oxides are in general coated with hydroxyl
groups when exposed to aqueous environments so
that hydroxylated metal oxides can cause a nucleophilic
attack [88].
Due to the method of analysis in a flame atomic
absorption spectrophotometer, no distinction was
made between the specific forms of the analyzed sub-
stances. No information obtained by this method can
specify whether copper/silver is released either in the
form of nanoparticles or ionic form, as observed by Dan-
kovich and Smith [43].
In this way, the combined effect of silver and copper
oxide nanoparticles caused the inactivation of virus
through their synergistic effect. One of the principal
mechanisms of biocidal action of these ions is thought
to be cell penetration. The positively charged copper
ions form electrostatic bonds with negatively charged
Figure 6. T4 bacteriophage inactivation in a continuous flow filtration experiment using GAC6 (GAC/Ag0.5%Cu1.0%) sample, with
220 L of percolated water. Values expressed by the average, with standard deviation.
ENVIRONMENTAL TECHNOLOGY 9
sites on the cell wall. The cell membrane is thus distorted,
allowing ingress of silver ions which attack the cell by
binding at specific sites to DNA, RNA, respiratory
enzymes and cellular protein, causing catastrophic
failure of the life support systems of the cell [89].
Results indicate that the filtration process with GAC6
(Ag0.5%Cu1.0%) is a potential technology of virus
removal for the production of drinking water. Silver
and copper are elements that, if ingested in excess, can
cause health damage, but silver and copper concen-
trations in the filtered water were 8.2 and 137.6 ppb,
respectively, which are below the limits stipulated by
the United States Environmental Protection Agency (US
EPA) for silver (100 ppb) [90] and copper (1000 ppb)
[43] in drinking water.
For the GAC6 (Ag0.5% Cu1.0%) sample, the filter life-
time was evaluated. As can be seen in Figure 6, the
sample had high inactivation efficiency up to 120 L,
achieving 4.95 log of viral inactivation. A decrease in
inactivation efficiency to 130 for 150 L, ranging from
2.51 to 2.96 log inactivation was observed. In the range
of 160–220 L, the inactivation was lower, ranging from
0.02 to 0.48 log viral inactivation.
The hypothesis of the present study is that the inacti-
vation mechanism prevails, T4 bacteriophage comes into
contact with silver and copper oxide embedded on the
surface of GAC and is inactivated during filtration.
Studies of Liga, Bryant [3] and Imai, Ogawa [49] demon-
strated that the inactivation may occur in a matter of
minutes in the presence of these metals. Concerning
the metal concentrations tested, the combination silver
and copper oxide demonstrated effectiveness in viral
inactivation and with further studies monitoring
10 Q. L. SHIMABUKU ET AL.
parameters such as color, pH, turbidity, chlorine, antibac-
terial activity, among other parameters, it is possible to
propose it as a filter for the obtainment of drinking
water and, consequently, be applied in household
filters, rural communities in developing countries and
in emergency situations of environmental disasters.
4. Conclusions
The process of GAC modification with silver and copper
oxide nanoparticles did not change the microporous
characteristic of the produced materials so that the
metals are the most responsible for viral removal and
inactivation of these produced materials. This study
reported a significant inactivation enhancement of T4
bacteriophage when the combination of silver and
copper oxide nanoparticles is used in comparison with
the use of a single metal. The concentrations tested
with the use of a single metal (Ag or Cu) were not
enough for viral inactivation.
The combined use of silver and copper oxide nano-
particles embedded in GAC presented a synergistic
effect in viral inactivation. Activated carbon is one of
the most utilized adsorbents worldwide, presents low
cost and is easy to obtain. The combination of activated
carbon with the studied metals enables the inactivation
of viruses, which is not achieved with conventional treat-
ment methods. As a consequence, this filter can be con-
sidered a promising material with a significant lifetime to
become a water purifier and be applied in water treat-
ment for the obtainment of drinking water.
Acknowledgements
The authors are grateful to COMCAP/UEM (Complexo de Cen-
trais de Apoio à Pesquisa) for DRX, TEM and SEM analyses.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
The authors gratefully acknowledge CAPES (Coordena-
ção de Aperfeiçoamento de Pessoal de Nível Superior)
for its financial support.
ORCID
Flávia Sayuri Arakawa http://orcid.org/0000-0003-1040-6170
Tânia Ueda-Nakamura http://orcid.org/0000-0001-5057-3518
References
[1] Shi CW, Wei J, Jin Y, et al. Removal of viruses and bacterio-
phages from drinking water using zero-valent iron. Sep
Purif Technol. 2012;84:72–78.
[2] Matsushita T, Suzuki H, Shirasaki N, et al. Adsorptive virus
removal with super-powdered activated carbon. Sep Purif
Technol. 2013;107:79–84.
[3] Liga MV, Bryant EL, Colvin VL, et al. Virus inactivation by
silver doped titanium dioxide nanoparticles for drinking
water treatment. Water Res. 2011;45:535–544.
[4] Simmons FJ, Kuo DHW, Xagoraraki I. Removal of human
enteric viruses by a full-scale membrane bioreactor
during municipal wastewater processing. Water Res.
2011;45:2739–2750.
[5] Kuo DHW, Simmons FJ, Blair S, et al. Assessment of human
adenovirus removal in a full-scale membrane bioreactor
treating municipal wastewater. Water Res. 2010;44:1520–
1530.
[6] Kitajima M, Haramoto E, Phanuwan C, et al. Detection of
genogroup IV norovirus in wastewater and river water in
Japan. Lett Appl Microbiol. 2009;49:655–658.
[7] da Silva AK, Le Saux J-C, Parnaudeau S, et al. Evaluation of
removal of noroviruses during wastewater treatment,
using real-time reverse transcription-PCR: different beha-
viors of genogroups I and II. Appl Environ Microbiol.
2007;73:7891–7897.
[8] Haramoto E, Katayama H, Oguma K, et al. Quantitative
analysis of human enteric adenoviruses in aquatic
environments. J Appl Microbiol. 2007;103:2153–2159.
[9] Kageyama T, Kojima S, Shinohara M, et al. Broadly reactive
and highly sensitive assay for norwalk-like viruses based
on real-time quantitative reverse transcription-PCR. J
Clin Microbiol. 2003;41:1548–1557.
[10] Ueki Y, Sano D, Watanabe T, et al. Norovirus pathway in
water environment estimated by genetic analysis of strains
from patients of gastroenteritis, sewage, treated wastewater,
river water and oysters. Water Res. 2005;39:4271–4280.
[11] Miagostovich MP, Ferreira FF, Guimarães FR, et al.
Molecular detection and characterization of gastroenteritis
viruses occurring naturally in the stream waters of Manaus,
central Amazonia, Brazil. Appl Environ Microbiol.
2008;74:375–382.
[12] Lodder WJ, Van Den Berg HHJL, Rutjes SA, et al. Presence
of enteric viruses in source waters for drinking water pro-
duction in The Netherlands. Appl Environ Microbiol.
2010;76:5965–5971.
[13] Vivier JC, Ehlers MM, Grabow WOK. Detection of entero-
viruses in treated drinking water. Water Res. 2004;38:2699–
2705.
[14] Papaventsis D, Siafakas N, Markoulatos P, et al. Membrane
adsorption with direct cell culture combined with reverse
transcription-PCR as a fast method for identifying entero-
viruses from sewage. Appl Environ Microbiol. 2005;71:72–79.
[15] Wegmann M, Michen B, Graule T. Nanostructured surface
modification of microporous ceramics for efficient virus
filtration. J Eur Ceram Soc. 2008;28:1603–1612.
[16] Blatchley ER, Gong W-L, Alleman JE, et al. Effects of waste-
water disinfection on waterborne bacteria and viruses.
Water Environ Res. 2007;79:81–92.
[17] Mamane H, Shemer H, Linden KG. Inactivation of E-coli,
B-subtilis spores, and MS2, T4, and T7 phage using UV/

H2O2 advanced oxidation. J Hazard Mater. 2007;146:479–
486.
[18] Aronino R, Dlugy C, Arkhangelsky E, et al. Removal of
viruses from surface water and secondary effluents by
sand filtration. Water Res. 2009;43:87–96.
[19] Jurzik L, Hamza IA, Puchert W, et al. Chemical and micro-
biological parameters as possible indicators for human
enteric viruses in surface water. Int J Hyg Environ
Health. 2010;213:210–216.
[20] Grabow W. Bacteriophages: update on application as
models for viruses in water. Water SA. 2001;27:251–268.
[21] Bales RC, Gerba CP, Grondin GH, et al. Bacteriophage
transport in sandy soil and fractured tuff. Appl Environ
Microbiol. 1989;55:2061–2067.
[22] Nasser AM, Glozman R, Nitzan Y. Contribution of microbial
activity to virus reduction in saturated soil. Water Res.
2002;36:2589–2595.
[23] Gutierrez L, Li X, Wang J, et al. Adsorption of rotavirus and
bacteriophage MS2 using glass fiber coated with hematite
nanoparticles. Water Res. 2009;43:5198–5208.
[24] Timchak E, Gitis V. A combined degradation of dyes and
inactivation of viruses by UV and UV/H2O2. Chem Eng J.
2012;192:164–170.
[25] Gerba CP. Applied and theoretical aspects of virus
adsorption to surfaces. Adv Appl Microbiol. 1984;30:133–
168.
[26] Templeton MR, Andrews RC, Hofmann R. Removal of par-
ticle-associated bacteriophages by dual-media filtration at
different filter cycle stages and impacts on subsequent UV
disinfection. Water Res. 2007;41:2393–2406.
[27] Zheng J, Zhao Q, Ye Z. Preparation and characterization of
activated carbon fiber (ACF) from cotton woven waste.
Appl Surf Sci. 2014;299:86–91.
[28] Depci T. Comparison of activated carbon and iron impreg-
nated activated carbon derived from Gölbaşı lignite to
remove cyanide from water. Chem Eng J. 2012;181–
182:467–478.
[29] Demirbas A. Agricultural based activated carbons for the
removal of dyes from aqueous solutions: a review.
J Hazard Mater. 2009;167:1–9.
[30] Tamai H, Yoshida T, Sasaki M, et al. Dye adsorption on
mesoporous activated carbon fiber obtained from pitch
containing yttrium complex. Carbon. 1999;37:983–989.
[31] ChangMing D, DongWei H, HongXia L, et al. Adsorption of
acid orange II from aqueous solution by plasma modified
activated carbon fibers. Plasma Chem Plasma Process.
2013;33:65–82.
[32] Tang D, Zheng Z, Lin K, et al. Adsorption of p-nitrophenol
from aqueous solutions onto activated carbon fiber.
J Hazard Mater. 2007;143:49–56.
[33] Zhou D, Hai R, Wang W, et al. Activated carbon fiber filler
in aerated bioreactor for industrial wastewater treatment.
Water Sci Technol. 2012;65:1753–1758.
[34] Hijnen WAM, Suylen GMH, Bahlman JA, et al. GAC adsorp-
tion filters as barriers for viruses, bacteria and protozoan
(oo)cysts in water treatment. Water Res. 2010;44:1224–
1234.
[35] Pelczar MJ, Reid RD, Chan ECS. Microbiologia. São Paulo:
McGraw-Hill; 1981.
[36] Khandelwal N, Kaur G, Chaubey KK, et al. Silver nanoparti-
cles impair Peste des petits ruminants virus replication.
Virus Res. 2014.
ENVIRONMENTAL TECHNOLOGY 11
[37] Lau B, Harrington G, Anderson M, et al. Removal of
nano and microparticles by granular filter media coated
with nanoporous aluminium oxide. Water Sci Technol.
2004;50:223–228.
[38] Jin S, Fallgren PH, Morris JM, et al. Removal of bacteria
and viruses from waters using layered double hydroxide
nanocomposites. Sci Technol Adv Mater. 2007;8:67–70.
[39] Wegmann M, Michen B, Luxbacher T, et al. Modification
of ceramic microfilters with colloidal zirconia to promote
the adsorption of viruses from water. Water Res.
2008;42:1726–1734.
[40] Mostafavi ST, Mehrnia MR, Rashidi AM. Preparation of nano-
filter from carbon nanotubes for application in virus
removal from water. Desalination. 2009;238:271–280.
[41] Bradley I, Straub A, Maraccini P, et al. Iron oxide amended
biosand filters for virus removal. Water Res. 2011;45:4501–
4510.
[42] Ahammed MM, Davra K. Performance evaluation of
biosand filter modified with iron oxide-coated sand for
household treatment of drinking water. Desalination.
2011;276:287–293.
[43] Dankovich TA, Smith JA. Incorporation of copper nanopar-
ticles into paper for point-of-use water purification. Water
Res. 2014;63:245–251.
[44] Yeddou AR, Chergui S, Chergui A, et al. Removal of
cyanide in aqueous solution by oxidation with hydrogen
peroxide in presence of copper-impregnated activated
carbon. Miner Eng. 2011;24:788–793.
[45] Lara HH, Ayala-Nuñez NV, Ixtepan-Turrent L, et al. Mode of
antiviral action of silver nanoparticles against HIV-1. J
Nanobiotechnol. 2010;8:1–8.
[46] Feng QL, Wu J, Chen GQ, et al. A mechanistic study of
the antibacterial effect of silver ions on Escherichia
coli and Staphylococcus aureus. J Biomed Mater Res.
2000;52:662–668.
[47] Elechiguerra JL, Burt JL, Morones JR, et al. Interaction of
silver nanoparticles with HIV-1. J Nanobiotechnol.
2005;3:1–10.
[48] Morones JR, Elechiguerra JL, Camacho A, et al. The bacteri-
cidal effect of silver nanoparticles. Nanotechnology.
2005;16:2346.
[49] Imai K, Ogawa H, Bui VN, et al. Inactivation of high and low
pathogenic avian influenza virus H5 subtypes by copper
ions incorporated in zeolite-textile materials. Antiviral
Res. 2012;93:225–233.
[50] Foster HA, Sheel DW, Sheel P, et al. Antimicrobial activity of
titania/silver and titania/copper films prepared by CVD. J
Photochem Photobiol A: Chem. 2010;216:283–289.
[51] Vainio U, Pirkkalainen K, Kisko K, et al. Copper and copper
oxide nanoparticles in a cellulose support studied using
anomalous small-angle X-ray scattering. Eur Phys J D-
Atom Mol, Opt Plasma Phys. 2007;42:93–101.
[52] Ben-Sasson M, Zodrow KR, Genggeng Q, et al. Surface
functionalization of thin-film composite membranes
with copper nanoparticles for antimicrobial surface prop-
erties. Environ Sci Technol. 2013;48:384–393.
[53] Clasen TF. Household water treatment and the millen-
nium development goals: keeping the focus on health.
Environ Sci Technol. 2010;44:7357–7360.
[54] Gerba CP, Naranjo JE, Jones EL. Virus removal from water
by a portable water treatment device. Wilderness Environ
Med. 2008;19:45–49.
12 Q. L. SHIMABUKU ET AL.
[55] Kumar VS, Nagaraja BM, Shashikala V, et al. Highly efficient
Ag/C catalyst prepared by electro-chemical deposition
method in controlling microorganisms in water. J Mol
Catal A: Chem. 2004;223:313–319.
[56] [56] Association APH. Standard methods for the examin-
ation of water and wastewater. 20th ed. Washington
(DC): American Public Health Association; 1998.
[57] Russel M, Lowman HB, Clackson T. Introduction to phage
biology and phage display. In: Clackson T, Lowman HB,
editors. Practical approach phage display. Oxford:
Oxford University Press; 2004. p. 1–26.
[58] Adams MH. Bacteriophages. New York (NY): Interscience;
1959. p. 450–454.
[59] Brady-Estévez AS, Nguyen TH, Gutierrez L, et al. Impact of
solution chemistry on viral removal by a single-walled
carbon nanotube filter. Water Res. 2010;44:3773–3780.
[60] Gerba CP, Naranjo JE. Microbiological water purification
without the use of chemical disinfection. Wilderness
Environ Med. 2000;11:12–16.
[61] Huang X, Dong W, Wang G, et al. Synthesis of confined Ag
nanowires within mesoporous silica via double solvent
technique and their catalytic properties. J Colloid
Interface Sci. 2011;359:40–46.
[62] Siriwardane RV, Poston Jr JA, Fisher EP, et al.
Decomposition of the sulfates of copper, iron (II), iron
(III), nickel, and zinc: XPS, SEM, DRIFTS, XRD, and TGA
study. Appl Surf Sci. 1999;152:219–236.
[63] Goscianska J, Nowicki P, Nowak I, et al. Thermal analysis of
activated carbons modified with silver metavanadate.
Thermochimica Acta. 2012;541:42–48.
[64] Srinivasan NR, Shankar PA, Bandyopadhyaya R. Plasma
treated activated carbon impregnated with silver nano-
particles for improved antibacterial effect in water disin-
fection. Carbon. 2013;57:1–10.
[65] Lam FLY, Hu X. A new system design for the preparation of
copper/activated carbon catalyst by metal-organic chemi-
cal vapor deposition method. Chem Eng Sci. 2003;58:687–
695.
[66] Parashar V, Parashar R, Sharma B, et al. Parthenium leaf
extract mediated synthesis of silver nanoparticles: a
novel approach towards weed utilization. Dig J
Nanomat Biostruct. 2009;4:45–50.
[67] Azam A, Ahmed AS, Oves M, et al. Size-dependent antimi-
crobial properties of CuO nanoparticles against Gram-
positive and-negative bacterial strains. Int J Nanomed.
2012;7:3527–335.
[68] Sing K, Everett D, Haul R, et al. Physical and biophysical
chemistry division commission on colloid and surface chem-
istry including catalysis. Pure Appl Chem. 1985;57:603–619.
[69] Freitas AF, Mendes MF, Coelho GLV. Thermodynamic
study of fatty acids adsorption on different adsorbents. J
Chem Thermodyn. 2007;39:1027–1037.
[70] Rivera-Utrilla J, Prados-Joya G, Sánchez-Polo M, et al.
Removal of nitroimidazole antibiotics from aqueous sol-
ution by adsorption/bioadsorption on activated carbon.
J Hazard Mater. 2009;170:298–305.
[71] Venkata Ramana DK, Yu JS, Seshaiah K. Silver nanoparti-
cles deposited multiwalled carbon nanotubes for
removal of Cu(II) and Cd(II) from water: surface, kinetic,
equilibrium, and thermal adsorption properties. Chem
Eng J. 2013;223:806–815.
[72] Gregory J. Approximate expressions for retarded van
der waals interaction. J Colloid Interface Sci.
1981;83:138–145.
[73] Hogg R, Healy TW, Fuerstenau DW. Mutual coagulation of
colloidal dispersions. Trans Faraday Soc. 1966;62:1638–
1651.
[74] Guy MD, McIver JD, Lewis MJ. The removal of virus by a
pilot treatment plant. Water Res. 1977;11:421–428.
[75] Scott TM, Sabo RC, Lukasik J, et al. Performance and cost-
effectiveness of ferric and aluminum hydrous metal oxide
coating on filter media to enhance virus removal. KONA
Powder Part J. 2002;20:159–167.
[76] Persson F, Långmark J, Heinicke G, et al. Characterisation
of the behaviour of particles in biofilters for pre-treatment
of drinking water. Water Res. 2005;39:3791–3800.
[77] Cookson Jr JT. Mechanism of virus adsorption on acti-
vated carbon. J Am Water Works Assoc. 1969;61:52–56.
[78] Stewart S, Fredericks PM. Surface-enhanced Raman spec-
troscopy of peptides and proteins adsorbed on an electro-
chemically prepared silver surface. Spectrochim Acta Mol
Biomol Spectrosc. 1999;55:1615–1640.
[79] Thurman RB, Gerba CP, Bitton G. The molecular mechan-
isms of copper and silver ion disinfection of bacteria
and viruses. Crit Rev Environ Sci Technol. 1989;18:295–
315.
[80] Auffan M, Rose J, Wiesner MR, et al. Chemical stability of
metallic nanoparticles: a parameter controlling their
potential cellular toxicity in vitro. Environ Pollut.
2009;157:1127–1133.
[81] Choi O, Hu Z. Size dependent and reactive oxygen species
related nanosilver toxicity to nitrifying bacteria. Environ
Sci Technol. 2008;42:4583–4588.
[82] Zodrow K, Brunet L, Mahendra S, et al. Polysulfone ultrafil-
tration membranes impregnated with silver nanoparticles
show improved biofouling resistance and virus removal.
Water Res. 2009;43:715–723.
[83] You J, Zhang Y, Hu Z. Bacteria and bacteriophage inacti-
vation by silver and zinc oxide nanoparticles. Coll Surf B:
Biointerfaces. 2011;85:161–167.
[84] Lund E. The significance of oxidation in chemical inacti-
vation of poliovirus. Archiv für die gesamte
Virusforschung. 1963;12:648–660.
[85] Shionoiri N, Sato T, Fujimori Y, et al. Investigation of
the antiviral properties of copper iodide nanoparticles
against feline calicivirus. J Biosci Bioeng. 2012;113:580–
586.
[86] Yamamoto N, Hiatt C, Haller W. Mechanism of inactivation
of bacteriophages by metals. Biochim Biophys Acta.
1964;91:257–261.
[87] Murray JP, Laband SJ. Degradation of poliovirus by
adsorption on inorganic surfaces. Appl Environ
Microbiol. 1979;37:480–486.
[88] Plastourgou M, Hoffmann MR. Transformation and fate
of organic esters in layered-flow systems: the role of
trace metal catalysis. Environ Sci Technol. 1984;18:756–
764.
[89] Hambidge A. Reviewing efficacy of alternative water treat-
ment techniques. Health Estate. 2001;55:23–25.
[90] Benn TM, Westerhoff P. Nanoparticle silver released into
water from commercially available sock fabrics. Environ
Sci Technol. 2008;42:4133–4139.