Chemosphere 146 (2016) 458e471

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Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

Inuence of milling on the adsorption ability of eggshell waste



, Jaroslav Brian
Matej Bala
z*, Jana Ficeriova
cin
Department of Mechanochemistry, Institute of Geotechnics, Slovak Academy of Sciences, Watsonova 45, 04001 Kosice, Slovakia

h i g h l i g h t s

g r a p h i c a l a b s t r a c t

Eggshell waste is an effective adsorbent of heavy metals.

The selectivity of the ESM toward
different ions was conrmed.

The effect of milling on the adsorption ability is different for ES and
ESM.

Two-fold morphology of the milled
ES was observed.

ES is suitable for the adsorption of
Ag(I) from the industrial waste.

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 11 October 2015
Received in revised form
24 November 2015
Accepted 1 December 2015
Available online 30 December 2015

Eggshell waste was successfully used for the removal of heavy metal ions from model solutions. The
effect of ball milling on the structure and adsorption ability of eggshell (ES) and its membrane (ESM) was
investigated, with the conclusion that milling is benetial only for the ES. The adsorption experiments
showed that the ESM is a selective adsorbent, as the adsorption ability toward different ions decreased in
the following order: Ag(I) > Cd(II) > Zn(II). The obtained Qm values for Ag(I) adsorption on the ESM and
ES were 52.9 and 55.7 mg g1, respectively. The potential industrial application of ES was also demonstrated by successful removal of Ag(I) from the technological waste.
2015 Elsevier Ltd. All rights reserved.

Handling Editor: Xiangru Zhang

Keywords:
Eggshell
Eggshell membrane
Adsorption
Silver
Cadmium
Milling

1. Introduction
The pollution of the environment is an actual issue with high
priority these days. Among its various types, the contamination of
water by heavy metal ions as a result of the industrial processes
taking place in the vast number of plants signicantly contributes

* Corresponding author.


E-mail address: balazm@saske.sk (M. Bala
z).
http://dx.doi.org/10.1016/j.chemosphere.2015.12.002
0045-6535/ 2015 Elsevier Ltd. All rights reserved.

to the to the overall pollution of the environment. Therefore, the

purication of these wastewaters is of high priority (Barakat, 2011;
Fu and Wang, 2011). Heavy metal ions are numerous, however for
this study, three particular were selected (namely cadmium(II),
silver(I) and zinc(II)). Cadmium(II) is one of the most dangerous
ones, as it represents a signicant hazard for human health (Godt
et al., 2006; Bernhoft, 2013). Silver is a noble metal, which has
been widely employed in the photographic and imaging industry
for many years. The accumulation of silver(I) ions in organisms
(including humans) through the food chain causes numerous


z et al. / Chemosphere 146 (2016) 458e471

M. Bala

List of symbols
BPR
b
ce
cs
E
ES
ESM
Kf
nf

Qm
qt
te
Xm

ball-to-powder ratio
constant of the Langmuir isotherm related to the
heat of adsorption (L.mg1)
equilibrium solution concentration of ions (mol.L1)
amount of the adsorbed ions (mol.g1)
free energy of adsorption
eggshell
eggshell membrane
Freundlich constant
constant representing the adsorption intensity of
the adsorbent qe-amount of ions adsorbed at
equilibrium (mg.g1)
maximum monolayer adsorption capacity (mg.g1)
amount of ions adsorbed at given time t (mg.g1)
time of equilibrium
adsorption capacity (mol.g1)

hl and Steinhoff, 1960; Rosenman

diseases and disorders (Schma
et al., 1979, 1987). Zinc(II) is the least dangerous from the selected
ions, as it is a major micronutrient in the human body (Hambidge
and Krebs, 2007). However, too much zinc(II) in the human body
can also cause serious problems like stomach cramps, anemia,
damage to the pancreas, etc. (Naito et al., 2010). Different methods
have been used for the effective removal of all these ions from
wastewater, among which the adsorption by biosorbents has an
inevitable place (Veglio and Beolchini, 1997; Mack et al., 2007;
Demirbas, 2008). Moreover, it was shown recently that after the
removal of Ag(I) by a biocompatible material, the Ag-laden sorbent
exhibits an antibacterial activity (Yao et al., 2013).
The eggshell is one of the most common biomaterials in nature.
It serves its important role in the development and production of
eggs (Hincke et al., 2011), however after the breakage of the egg and
removal of the inner content used further, the eggshell waste is
very often simply discarded and disposed at landlls. The eggshell
waste comprises the eggshell (ES) itself and the eggshell membrane
(ESM). It represents 11% of the total weight of the egg. The main
component of the ES is calcite CaCO3 (94%). Other components
include MgCO3 (1%), Ca3(PO4)2 (1%) and organic matter (4%)
(Stadelman, 2000). The ESM is a brous proteinous structure which
serves its unique purpose within the egg (Nys et al., 2004). Despite
being treated as a waste, both components have multidisciplinary
applications. The ES can be used, e.g. as a source of calcium for the
synthesis of hydroxyapatite (Gergely et al., 2010), as a precursor for
composite materials (Ghani and Young, 2010) or as a source of
calcium oxide for the sorption of CO2 (Mohammadi et al., 2014). The
ESM is suitable for a wide spectrum of applications too which were


recently reviewed in Bala
z (2014). Namely its use as a biotemplate
(Su et al., 2008) or biosensor (Li et al., 2008) can be mentioned. Both
discussed biomaterials can be also utilized as a biosorbent of heavy
metal ions (Suyama et al., 1994; Park et al., 2007; Shimada et al.,
2010; Ahmad et al., 2012; Daraei et al., 2013; Flores-Cano et al.,
2013; Shaheen et al., 2013). The ESM was reported to exhibit a
signicant selectivity toward different heavy metal ions, due to
which it could be used as a stationary phase in a column chromatography (Ishikawa et al., 2002). The adsorption of cadmium(II)
(Kuh and Kim, 2000; Koumanova et al., 2002; Cheng et al., 2011a;
Flores-Cano et al., 2013) and silver(I) (Cheng et al., 2011b; Ho
et al., 2014) on both discussed biomaterials is of particular interest. The adsorption of zinc(II) of the ES was studied extensively (de
Paula et al., 2008; Shaheen et al., 2013), however the successful

459

adsorption of zinc(II) on the ESM was not reported until now.

The adsorption ability of the bio-sorbents can be increased by

et al., 2010; Leyva-Ramos et al., 2012;
their modication (Orolinova
Wang et al., 2013; Suresh et al., 2014). Milling is one of the effective
a

kova

et al., 2013). It can be generally
methods (Bal

a
z, 2000; Bujn
said that the inuence of milling on cation-exchange properties of
sorbents is practically unexplored, with exception of few papers
(Montinaro et al., 2007; Janusz et al., 2010; Bal

a
z et al., 2015a).
Depending on the intensity of milling, it is possible to only slightly
activate the sample, or to perform reactions which need a large




quantum of energy supply in order to proceed (Bala
z, 2008; Bala
z
et al., 2013b). The potential of milling to increase the adsorption


ability of the eggshell was reported very recently (Bala
z et al.,
2015a), however the effect of milling on the ESM was not investigated until now.
The aim of this study was to investigate the effect of milling of
the eggshell waste biomaterials on their adsorption ability toward
silver(I) ions. Although quite similar study was published recently
(Ho et al., 2014), the novelty in this paper lies in the introduction of
milling procedure and analyzing the results in more detail by
applying Langmuir and Freundlich models to describe the adsorption process. The real application of the ES to remove silver(I) from
the technological waste and the impact of mild milling on the
physico-chemical properties of the ESM were also investigated.
Moreover, the ESM was used also for the adsorption of cadmium(II)
and zinc(II) ions to conrm its selectivity. Finally, the desorption
behavior of the metal-laden ESM is reported and the adsorption
ability of the two studied materials is compared in detail. The main
idea of this paper is to show that the eggshell waste represents an
interesting selective material for the potential removal of heavy
metal ions from wastewaters and should not just be discarded.
2. Materials and methods
2.1. Materials
Raw eggshell containing the eggshell membrane was provided
by a selected canteen in Kosice. The pure ES and ESM were collected
by the same procedures, as were described in our previous works




((Bala
z et al., 2013a) and (Bala
z et al., 2015a), respectively). Cadmium nitrate tetrahydrate Cd(NO3)2.4H2O (ITES, Slovakia), silver
nitrate AgNO3 (Merck Millipore, Germany), zinc nitrate hexahydrate Zn(NO3)2.6H2O (Sigma-Aldrich, United Kingdom), sodium
hydroxide NaOH (ITES, Slovakia) and nitric acid HNO3 (ITES,
Slovakia) were used as chemicals without further purication. The
technological waste containing silver(I) ions was obtained from the
company DOMA, a.s., Presov and its chemical composition was
analyzed by atomic absorption spectroscopy.
2.2. Milling
The milling of both biomaterials was peformed in a laboratory
planetary ball mill Pulverisette 6 (Fritsch, Germany) under slightly
different conditions. The common conditions comprised the
following: loading of the mill- 50 balls of 10 mm diameter; ball
charge in the mill- 360 g; material of the milling chamber and ballstungsten carbide; atmosphere-air; laboratory temperature.
The differences were in rotation speed of the planet carrier (i.e.
milling speed), sample mass, milling time and ball-to powder ratio
(BPR). These conditions are listed in Table 1.
In order to clearly label the different ES/ESM samples discussed
within the paper, the numbers describing the duration of milling
are given immediately after the abbreviation ES or ESM, e.g. the
abbreviation ESM0 corresponds to the non-milled ESM, ES360
stands for the ES milled for 360 min, etc.


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460

Table 1
Different milling conditions used for treatment of eggshell and eggshell membrane.
Biomaterial

Sample mass [g]

Milling time [min]

Milling speed [min1]

Ball-to-powder ratio

ES
ESM

5
3

0e360
0e30

500
100

72
120

The milling ran in batch mode, so for each experiment, a new

sample was provided.
2.3. Characterization
2.3.1. Specic surface area measurements
The specic surface area was determined by the lowtemperature nitrogen adsorption method using NOVA 1200e Surface Area & Pore Size Analyzer (Quantachrome Instruments, United
Kingdom). The values were calculated using the BET theory.

In the case of the desorption tests, the selected metal-laden

samples after the adsorption process were dried and separated
into three fractions. The samples were then put into distilled water
(the amount of used water was such that the concentration of the
metal-laden ESM was 1 g L1) and mixed for different time (30, 120
and 360 min). After this process, the suspension was ltered
through the lter paper and the ltrate was analyzed in the same
way as in the case of adsorption tests.

3. Results and discussion

2.3.2. Infrared spectroscopy
The infrared spectra in the frequency range 4000e650 cm1
were obtained by using a FTIR spectrometer Tensor 29 (Bruker,
Germany) by applying the ATR method.
2.3.3. Scanning electron microscopy
The morphology of the samples was analyzed using a MIRA3 FESEM microscope (TESCAN, Czech Republic) equipped with the EDX
detector (Oxford Instrument, United Kingdom). The majority of the
ESM samples were coated with the layer of carbon in order to
eliminate their undesirable charging.
2.3.4. Zeta potential
The zeta potential was measured using a Zetasizer Nano ZS
(Malvern, United Kingdom). For each measurement, 10 mg of ES/
ESM was put into 10 mL of distilled water or metal (Ag, Cd or Zn)
nitrate solution with the concentration of 200 mg L1. The measurement was conducted within the pH range 2e13, which was
adjusted by the addition of 0.1 M HNO3 or 0.1 M NaOH.
2.4. Adsorption and desorption tests
The adsorption ability of the ESM was investigated on model
solutions of chemically pure AgNO3, Cd(NO3)2.4H2O and
Zn(NO3)2.6H2O in distilled water with the desired concentration.
The adsorption of silver(I) ions was pursued in the concentration
range 10e200 mg L1 and for the cadmium(II) ions, the range
10e150 mg L1 was examined. For the zinc(II) adsorption, only the
concentration 200 mg L1 was used. The adsorbent concentration
was 1 g L1. The adsorption experiments were performed in
Erlenmeyer's asks placed on a laboratory shaker for a different
time (until the equilibrium was reached) at a laboratory temperature. The pH was adjusted by the addition of 0.1 M HNO3 or 0.1 M
NaOH into the solution. The solutions were then ltered through
the lter paper and the ltrate was analyzed with respect to the
content of residual metal ions using an atomic absorption spectrometer SPECTRAA L40/FS (Varian, Australia).
The adsorption ability of the ES toward Ag(I) was investigated
using the same experimental setup as described for the ESM. The
effect of milling was investigated on a model solution of Ag(I) ions
with the concentration of 200 mg L1. For the adsorption at
different concentrations, the concentration range between 10 and
150 mg L1 was used. The adsorption of Ag(I) from waste was
performed using the ES sample milled for 360 min and the kinetics
of the process was studied by measuring the amount of adsorbed
silver(I) ions in different adsorption times (1e240 min).

The industrial eggshell waste comprises two components-the

eggshell (ES) and the eggshell membrane (ESM). As enough
attention was devoted to the characterization and adsorption


ability of the milled ES in our previous studies (Bala
z et al., 2013c,
2015a, 2015b), the effect of milling was investigated in detail only
for the ESM.
The unique brous structure of the ESM is the most important


characteristics for its potential applications (Bala
z, 2014). Therefore the effect of high-energy milling (HEM), during which normally high milling velocities (e.g. 500e800 rpm) are applied,
would be most probably negative, as the unique brous structure
would be certainly destroyed. Because of that, we applied very
mild milling (100 rpm) and we hoped that the brous structure
would be maintained, at least to some extent. We hypothesized


that such a slight mechanical activation (Bala
z, 2000) could
possibly enhance the properties of the ESM, namely the adsorption
ability toward heavy metal ions, as it was achieved in the case of
the ES (Bal

a
z et al., 2015a). Our hypothesis was supported by the
work by Ishikawa et al. (2002), in which the positive effect of
powdering of the ESM was denitely conrmed. The impact of
mild milling on the ESM was pursued by the specic surface area
measurement, IR spectroscopy and SEM. Namely the ESM milled
for 30 min (labeled ESM30) was compared with the non-milled
ESM (ESM0).

3.1. Comparison of the physico-chemical properties between the

non-milled and milled ESM
3.1.1. Specic surface area measurements
The value of the specic surface area SA 13.2 m2.g1 of the
non-milled ESM is signicantly higher than in the case of the nontreated eggshell (0.5 m2.g1 (Tsai et al., 2008)), thus suggesting the
richer pore properties of the ESM. The SA value was changing with
the time of milling. However, it did not increase, as in the case of the


eggshell (Bala
z et al., 2015a), but the decrease was observed. From
the initial value, it decreased to 2.4 m2.g1 after 5 min of milling
and further decrease to 0.7 m2.g1 was evidenced for the sample
ESM30. This is understandable, since the ESM can be categorized as
high-dispersed solid and the aggregation processes may prevail
over the dispersion even under mild milling (Sydorchuk et al.,
2010). When soft materials are treated, the energy is absorbed in
deformation processes (Butyagin, 1989), which is also the case of
the ESM. As the bers are mangled during milling, the surface is
signicantly compressed, which results in the reduced SA value.


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3.1.2. Infrared spectra

In order to determine, whether chemical changes take place
during the milling, the infrared spectra of the samples ESM0 and
ESM30 were recorded. They are presented in Fig. 1.
The infrared spectrum of the ESM can be divided into two
regions-the rst one between 3750 cm1 and 2500 cm1 and the
other one below 1700 cm1. In the region with higher wavelengths,
the most intensive peak is evidenced at 3287 cm1, which corresponds to the stretching mode of NeH bonds (Rath et al., 2014). The
peaks at 3060 cm1, 2932 cm1, and 2869 cm1 correspond to the
asymmetric stretching vibrations of the CeH bonds present
in CeH and CH2 groups (Kaiden et al., 1987; Weymuth et al.,
2010). In the region with lower wavelengths, the peaks at
1630 cm1 (C]O), 1530 cm1 (CeN stretching/NeH bending
modes), and 1234 cm1 (CeN stretching/NeH bending modes) can
be assigned to the amide I, amide II, and amide III vibrations of the
glycoprotein mantle of the bers, respectively (Bandekar, 1992;
Arami et al., 2006; Dong et al., 2007; Kong and Yu, 2007). The
peaks at 1448 cm1, 1073 cm1 and 620 cm1 correspond to the
stretching modes of C]C, CeO and CeS bonds, respectively (Dong
et al., 2007; Gunasekaran and Sailatha, 2008; Liu et al., 2008; Zhao
and Chi, 2009; Whitehead et al., 2011).
It can be seen that all the mentioned peaks are present in the
spectra of both ESM0 and ESM30, so no chemical changes occur as a
result of mild milling. The only difference is the presence of small
double peak around 2350 cm1 in the spectrum of ESM30, which is
a result of the vibrations of the adsorbed molecules of atmospheric
CO2, but this has nothing to do with potential chemical changes in
the ESM.
3.1.3. Zeta potential
In order to check whether or not milling caused the changes in
the charge of the surface layer of the ESM, zeta potential values at
different pH for the samples ESM0 and ESM5 are compared in Fig. 2
below.
It can be seen from the gure that milling did not bring about a
signicant change in the value of ZP, so also the surface charge
distribution should be more-or-less maintained after the mild
milling, which further conrms that no chemical changes occur in
the ESM during this procedure.

461

Fig. 2. The inuence of milling on zeta potential: the dependence of zeta potential on
the pH for ESM0 and ESM5.

3.1.4. Scanning electron microscopy

Milling denitely affects the morphology of the ESM. It could be
seen with the naked eye that the ake-like structure, which was
present before milling was maintained also in the case of the milled
samples, only the akes seemed smaller in the latter case. By the
means of SEM, the effect of mild milling on the morphology of the
bers of the ESM was investigated (Fig. 3).
Although the gures are of different quality due to the different
sample preparation, the differences can denitely be seen. Whereas
in Fig. 3a, the long non-touched bers of various diameter can be
observed, the mangled and crushed bers are visible in Fig. 3b. It is
a proof that during milling, the bers are exposed to various forces,
causing them to deform and then lead to their rupture and
compression into circle shapes. In Fig. 3b, two different morphologies can be observed. Whereas in the upper right part, the surface
layer of the ake can be seen and no individual bers can be further
distinguished, in the lower left part, the residues of the torn bers
can still be observed. For better understanding, the magnied SEM
images of both these regions were recorded (Fig. 4).
In Fig. 4a, where the residues of the bers from the bulk of the
ake are shown, the effect of milling is not so pronounced. Some
bers maintained their structure, although there are small lumps
present on them. In the upper part, it seems that one ber is
starting to be wrapped by the residues of some other bers. Maybe
this is the mechanism how the surface lump-like layer, the
morphology of which is shown in Fig. 4b, is formed. The lumps at
this surface layer are of various sizes, so it is possible that rstly the
small ones are formed and as the milling proceeds, they are getting
larger, as more residues of the bers are incorporated into them. No
bers can be observed at the surface of the ake, as the milling balls
have totally destroyed the original morphology there.
3.2. Adsorption of heavy metal ions on the ESM
The ESM was used for the adsorption of three selected metal
ions from their water solutions (namely cadmium(II), silver(I) and
zinc(II)).

Fig. 1. The infrared spectra of the ESM: black lineenon-milled; red lineemilled for
30 min. (For interpretation of the references to colour in this gure legend, the reader
is referred to the web version of this article.)

3.2.1. Optimization of pH
Firstly, zeta potential was measured, in order to determine the
most suitable pH value for the adsorption. The dependences of ZP

462

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M. Bala

Fig. 3. The SEM images of the samples: (a) ESM0; (b) ESM30.

Fig. 4. The SEM images of the sample ESM30: (a) the bers inside the ake; (b) the surface of the ake.

on pH for all three ions are presented in Fig. 5aec.

It can be seen that in all the studied cases, excluding the area of
high pH values for Ag(I) adsorption (right part of Fig. 5a), a shift
toward the positive values of zeta potential was observed after
immersing the ESM into all studied metal ion solutions. This is a
consequence of the presence of larger amount of positively charged
metal ions near the surface of the sorbent. The pH, at which the
largest difference between the ZP values of ESM in water and in
corresponding salt was recorded was considered optimum. However, as in the case of Cd(II) (Fig. 5b) and Zn(II) (Fig. 5c), it was pH 8
and there would be a danger of the precipitation of metal hydroxides (Chen, 2010), pH 7 was applied for these two ions. For
Ag(I), pH 6 was satisfactory (Fig. 5a).
3.2.2. Selectivity tests
After the determination of the most appropriate pH, the
adsorption tests for all three ions were performed with the nonmilled ESM. The adsorption ability (represented by the value qt)
toward each ion is shown in Fig. 6.

It can be seen from the gure that the ESM exhibits a selectivity
towards different ions, thus conrming the facts presented in
Ishikawa et al. (2002). It was found that the adsorption ability of the
non-treated ESM toward cadmium(II) lies in between the ones
toward silver(I) and zinc(II) ions. The adsorption ability toward
silver(I) is the highest, while zinc(II) is not adsorbed. It was
concluded that the ESM is not capable of Zn(II) ions adsorption, so
further considerations in the paper are related only to the
adsorption of silver(I) and cadmium(II) ions.
3.2.3. Inuence of milling
The inuence of mild milling was evaluated for the adsorption
of Ag(I) and Cd(II) ions. The results are presented in Fig. 6.
It can be seen from the gure that mild milling has a negative
inuence on the adsorption ability, unlike in the case of the
eggshell (Bal

a
z et al., 2015a). In the case of Ag(I) (Fig. 7a), this
negative inuence becomes evident after 5 min of milling, whereas
in the case of Cd(II) (Fig. 7b), it takes longer time to express. It
becomes signicant after 30 min of milling. These results did not


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463

Fig. 5. The dependence of zeta potential on the pH for ESM in water (black) and in corresponding metal nitrate solution (red): (a) Ag; (b) Cd; (c) Zn (cM 200 mg L1). (For
interpretation of the references to colour in this gure legend, the reader is referred to the web version of this article.)

the active sites, only exposing more of them, thus resulting in

higher adsorption ability. Nevertheless, although milling did not
bring about the improvement of the adsorption ability of the ESM,
the non-milled ESM was investigated further.
3.2.4. Adsorption isotherms
The adsorption isotherms for the adsorption of Ag(I) and Cd(II)
on the non-treated ESM are shown in Fig. 8.
The shape of the adsorption isotherms for two studied ions in
the studied concentration range is different. Whereas for Ag(I), a
plauteau can be observed for concentrations higher than 80 mg L1,
in the case of Cd(II), more-or-less constant increase of the
adsorption ability as the concentration increases can be observed.
These results hint to the potential different mechanism of the
adsorption.

Fig. 6. The adsorption of Ag(I), Cd(II) and Zn(II) ions on the non-milled ESM
(cM 200 mg L1 pHAg,Zn 6, pHCd 7).

support our hypothesis about the improved adsorption ability as a

result of milling based on the positive effect of particles miniaturization reported in Ishikawa et al. (2002). It is highly probable that
the active sites were destroyed despite the application of very mild
milling in our case. On the other hand, cutting and minimizing the
particle size by the laboratory blender performed within the work
(Ishikawa et al., 2002) most probably did not affect the structure of

3.2.5. Comparison of Langmuir and Freundlich parameters

These data were used for the evaluation of the Langmuir and
Freundlich parameters. The linearized forms of Langmuir and
Freundlich isotherms were applied (Eqs. (1) and (2), respectively).

Ce
1
Ce

qe Qm b Qm

(1)

where ce and qe are the equilibrium solute concentration [mg.L1]

and the equilibrium adsorption capacity [mg.g1], respectively, Qm
is the Langmuir constant representing the maximum monolayer
adsorption capacity (amount of adsorbed metal ions per 1 g of
sorbent as a monolayer) and b is the constant of the Langmuir


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464

Fig. 7. The inuence of mild milling on adsorption ability of ESM toward: (a) Ag(I); (b) Cd(II) (cM 200 mg L1, pHAg 6, pHCd 7).

Fig. 8. The adsorption isotherms for metal ions adsorption on the ESM: (a) Ag(I); (b) Cd(II).

isotherm related to the heat of adsorption [L.mg1].

ln cs ln Kf nf ln ce

(2)

where cs is the amount of the adsorbed metal ion [mol.g1]; ce is the

equilibrium solution concentration of metal ion [mol.L1]; Kf is the
Freundlich constant [mol.g1], nf is a constant representing the
adsorption intensity of the adsorbent.
The results obtained by applying these models for both studied
ions and the corresponding parameters are presented below in
Fig. 9 and Table 2, respectively.
Interesting conclusions can be drawn from the gure and table.
Whereas for the adsorption of silver(I), the Langmuir model is more
suitable, the Freundlich model is more suitable for cadmium(II)
adsorption. This is, of course, connected with the different shapes of
the adsorption isotherms presented in Fig. 8. It is possible that
different mechanism is taking place for the adsorption of each ion.
In Koumanova et al. (2002), it is stated that the suitability of the
Langmuir model conrms the chemisorption, so it seems that silver
should be adsorbed non-reversibly. However, the correlation coefcient for the Langmuir model in the mentioned paper was only
0.76 and it was 0.85 for the Freundlich model, so it seems that the
latter model is more suitable also in their case. Nevertheless, our
results further conrm the selectivity of the ESM toward different
ions and the obtained Qm value, namely for the adsorption of Ag(I)

ions is comparable to other natural or modied biosorbents (Coruh

et al., 2010; Lihareva et al., 2013; Sari and Tuzen, 2013). In order to
elucidate the reversibility/irreversibility of the adsorption, the
desorption experiments were performed (part 3.4).
3.2.6. Characterization of products after adsorption
The ESM after the adsorption of Ag(I) and Cd(II) ions was
characterized by FTIR and SEM. No differences could be observed
before and after the adsorption of both ions in the FTIR spectra and
therefore, they are not provided. Also no hypothesis about the
particular functional groups of the ESM involved in the adsorption
can be stated.
Using the SEM microscopy, elemental mapping was performed
and EDX spectra were collected for the sample after the adsorption
of both ions. The results for the adsorption of Ag(I) and Cd(II) are
shown in Figs. 10 and 11, respectively. Carbon label was removed
from both gures (the sample was coated with it in order to avoid
unwanted charging by the electron beam), as it could cause some
confusion, if it was maintained within the results. However, the
main peaks of carbon can be seen in both EDX spectra (the most
intensive peaks).
3.2.6.1. Ag-laden ESM. In Fig. 10a, the EDS layered image
comprising all the elements is shown. The individual mapping for
O, S and Ag is presented in Fig. 10bed, respectively. At the rst


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465

Fig. 9. The linearized adsorption isotherms for the adsorption of metal ions on the ESM: (a) Langmuir, Ag(I); (b) Freundlich, Ag(I); (c) Langmuir, Cd(II); (d) Freundlich, Cd(II).

Table 2
The parameters for the adsorption of silver(I) and cadmium(II) ions on the ESM
obtained by applying various models.
Ion

Langmuir model
Qm [mg.g

Ag(I)
Cd(II)

52.910
23.419

1

b [mg.g
0.270
0.037

Freundlich model
1

R2l

KF [mmol.g1]

nf

R2f

0.9956
0.9002

4.468
6.935

0.314
0.531

0.9494
0.9974

glance it seems that the mapping results are inconsistent, as the

distribution of individual elements differs signicantly. However, it
is known that the difference in the depiction of elemental distribution is dependent on the atomic number and that the exact
localization of lighter elements is more precise than in the case of
heavy elements. Therefore it seems that oxygen is located exactly
on the bers, as it is the lightest element from the studied ones. On
the other hand, the adsorbed Ag is heavy element and therefore it
seems that its distribution is completely homogeneous and not
connected to the ESM bers at all. However, its presence in the
system is undeniable. In the EDX spectra (Fig. 9e), the same elements can be observed. These results represent the proof of the
successful adsorption of Ag(I) on the ESM.
3.2.6.2. Cd-laden ESM. The results for the cadmium(II) adsorption
are quite similar to the ones obtained for the adsorption of silver(I).
The homogeneous distribution of Cd, which can be seen mainly in
Fig. 11d can be explained by the same effect of heavy element
mentioned for silver. The EDX spectrum in Fig. 11e looks also similar
as in the case of Ag(I) adsorption, however the amount of the

adsorbed metal, compared to silver is signicantly lower (in the

case of Ag, it was 27.9% and for Cd it is only 10.9%). The results are
comparable, as the values for the elements O and S are more-or-less
the same in both cases. The obtained results are in accordance with
the observations made from the adsorption tests, in which also the
larger amount of silver(I), in comparison with cadmium(II), was
adsorbed.

3.3. Desorption tests

In order to determine the stability of the ESM-metal ion system,
the desorption tests were performed. The results for both ions are
presented in Table 3.
It can be seen that the percentual amount of both desorbed
metals is low, however it slightly increases with the desorption
time. The difference in the behavior of the two ions can be
observed.
The results with the desorption of Ag(I) have shown almost
negligible values of the desorbed metal within the rst two hours.
Although the higher value was observed in the case of the sample
desorbed for 30 min, the difference is within the range of a measurement error. However, 3.5% desorbed Ag(I) after six hours
cannot be neglected. It seems that silver(I) ions are adsorbed quite
strongly on the ESM, so a possible chemical adsorption can take
place. However, as it partly leaks into water, the process cannot be
considered completely chemical, but in general it can be stated that
the desorbed values are low.
The results with the Cd-laden ESM have shown that a small
amount of cadmium(II) is released into the solution and in


z et al. / Chemosphere 146 (2016) 458e471

M. Bala

466

Fig. 10. Surface characterization of the ESM after the adsorption of Ag(I): (a) SEM with EDS layered image; elemental mapping: (b) oxygen; (c) sulphur; (d) silver; (e) EDX spectrum.

Fig. 11. Surface characterization of the ESM after the adsorption of Cd: (a) SEM with EDS layered image; elemental mapping: (b) oxygen; (c) sulphur; (d) cadmium; (e) EDX
spectrum.

Table 3
Results of desorption tests.
Desorption time [min]

Desorbed amount of ion [mg L1]

Ag(I)

Adsorbed
30
120
360

Cd(II)

[mg.L1]

[%]

[mg.L1]

[%]

59.7
0.65
0.43
2.09

e
1.09
0.72
3.50

11.3
0.15
0.33
0.71

e
1.33
2.92
6.28

comparison to Ag(I) release, the values are higher. The value after
6 h is 1.8-fold higher than in the case of Ag(I). It hints to the fact,

that the binding is weaker in the present case and that the potential
chemical adsorption is taking place to a smaller extent. Thus the
adsorption process cannot be considered irreversible, on the con

trary to the adsorption of Cd(II) on the ES (Bala
z et al., 2015a). This
follows the different chemical composition of the ES and ESM.
In summary, it can be concluded that the desorption process
occurs in the case of both ions, and in comparison with other sorbents (Lata et al., 2015), the values are low. The process of irreversible adsorption is more signicant in the case of Ag(I), thus
supporting the hypothesis about the chemisorption based on the
better suitability of the Langmuir model. Of course, it can be hypothesized that if the desorption time would be long enough, all
the adsorbed species would be desorbed, but we consider this
improbable, as the desorbed values after 6 h are low. However, no


z et al. / Chemosphere 146 (2016) 458e471

M. Bala

467

denite conclusions can be made and further studies would be

necessary in order to elucidate the exact role and share of reversible
and irreversible adsorption.
3.4. Adsorption of silver(I) ions on eggshell
As the adsorption of silver(I) ions on the ESM was the best
among the studied heavy metal ions, we have decided to compare it
with the adsorption ability of the ES.
3.4.1. Optimization of pH
To nd out which pH would be the most suitable for the sorption
of Ag(I) ions on the ES, the measurements of zeta potential at
different pH for the milled ES both in water and in silver nitrate
solution were carried out. The results are shown in Fig. 12.
The differences in the zeta potential values in the case of water
and silver nitrate solutions are obvious. The shift toward the more
positive ZP values was observed again in the presence of the salt
solution, similarly to the ESM. It can be seen from the gure that
both high and low pH are not suitable for the adsorption, as in the
rst case, AgOH starts to precipitate at pH between 7 and 8 (Chen,
2010) and in the latter case, the CaCO3 from the ES is signicantly
dissolved (Flores-Cano et al., 2013). The value of zeta potential at pH
5 in the water solution was 11.3 mV, whereas in the case of silver
nitrate solution, it was 3.8 mV. The difference between zeta potential values in this case was the highest and therefore this pH was
selected for the sorption experiments.
3.4.2. Inuence of milling
The kinetics of the adsorption of Ag(I) on the ES was studied on
three selected ES samples. The results are presented in Fig. 13.
As can be seen in the gure, the milling for 60 min did not bring
about the increase of the adsorption ability at all, as the results for
the non-treated sample and the sample milled for 60 min were
almost identical- the amount of the adsorbed silver(I) ions was
around 40 mg.g1 for both samples. The sorption process was
very fast, because the values of Ag(I) uptake were almost the same
from the rst measurement after 5 min and did not vary much as
the sorption progressed. On the other hand, milling for 360 min
lead to a signicant effect- more than two-fold increase in sorption
ability was observed. This could be in connection with the

Fig. 12. The dependence of the zeta potential of the sample ES360 on pH in water and
in silver nitrate solution (cAg 200 mg L1).

Fig. 13. The inuence of milling time on the adsorption ability of ES towards Ag(I)
(cAg 200 mg L1, pH 5).

increasing amount of aragonite phase in the milled ES, as its inuence was denitely conrmed in the case of cadmium and was


discussed in detail in Bala
z et al. (2015a). It is possible that calcite
itself is not a good adsorbent of Ag(I), while aragonite is (Demina


et al., 2012). According to Bala
z et al. (2015a), there is 7.5%
and 54.9% aragonite in the ES milled for 60 min and 360 min,
respectively, so it is possible that some critical amount of aragonite
phase necessary for the improved adsorption ability toward silver(I) ions to show. The change in the values of the specic surface
area is not a key parameter, similarly as in the case of cadmium(II)
adsorption.
3.4.3. Adsorption isotherms
To calculate the maximum adsorption capacity of the ES milled
for 360 min, the experiments with different concentrations were
performed. According to the kinetics study, the sorption time of
240 min seemed appropriate. The adsorption isotherm is shown in
Fig. 14.
The shape of the isotherm is quite similar to that of the
adsorption of Ag(I) ions on the ESM, with a plateau in the area of
higher concentrations.

Fig. 14. The adsorption isotherm for Ag(I) ion adsorption on the sample ES360.

468

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M. Bala

3.4.4. Comparison of Langmuir and Freundlich parameters

The obtained dependance was linearized by applying both
Langmuir and Freundlich models. The linearized curves and the
corresponding parameters are summarized in Fig. 15 and Table 4.
It can be seen from the results that Langmuir model accurately
describes the process, while Freundlich model does not. From our
point of view, the obtained value of maximum adsorption capacity
55.7 mg.g1 is high enough to be interesting for further environmental applications.

3.4.5. Adsorption of Ag(I)-containing waste

To show the application potential of the milled ES in technology,
the adsorption tests on the technological waste containing silver(I)
were performed, using the sample ES360 (sample with the best
results in the kinetic study). The concentrations of all cations
detected in the waste are presented in Table 5.
It can be seen that the major component of the waste is chromium. Potassium, silver and zinc are almost of equal amount, all
being present in tens of mg.mL1. Also the contribution of another
minor constituents present in the ng.mL1 scale cannot be
neglected. The adsorption of chromium on the ES was investigated
recently (Daraei et al., 2015; Kumaraswamy et al., 2015) with
the conclusion that chromium can be effectively adsorbed. Therefore its vast abundancy in the present waste might be of great
signicance and certainly affects the adsorption of silver(I). A
signicant amount of potassium and zinc would also denitely
inuence the adsorption ability of the ES, representing the candidates for the potential competition for the active sites. Despite
all these facts, only the adsorption of silver(I) was pursued in order
to compare the results with the Ag(I) adsorption from the model
solution.
The results of sorption kinetics are presented in Fig. 16 below.
It can be seen from the gure that almost half of Ag(I) ions
present in the waste (the measured qt value was 28.59 mg Ag(I)/g
ES) was adsorbed immediately (after 1 min) by the milled ES and
this amount did not vary much with the increasing sorption time.
However, slight increase was evidenced in the case of longer
adsorption times. The nal qt value after 240 min was 37.41 mg
Ag(I)/g ES. The lower value in comparison with the model solutions
can be explained by the presence of other ions in the waste, which
compete for the adsorption sites with the Ag(I) ions. However, the
possibility of utilizing the ES biomaterial for the industrial application is denitely conrmed.

Table 4
The parameters for the adsorption of silver(I) on the sample ES360 obtained by
applying various models.
Langmuir model

Freundlich model

Qm [mg.g1]

b [mg.g1]

R2l

Kf [mmol.g1]

nf

R2f

55.7

0.68

0.9983

2.203

0.192

0.7470

Table 5
The cations present in waste.
Major cations

Concentration [mg.mL]

Minor cations

Concentration [ng.mL]

Cr
K
Ag
Zn

481.3
62.9
54.71
45.7

Fe
Mn
Al
Na
Ni
Pb
Cu
Co

345
236
66
14
10
5
5
0.5

Fig. 16. The adsorption of Ag(I) by the sample ES360 from the technological waste.

3.5. The comparisons

Within this study, a lot of collected data can be compared by

Fig. 15. The linearized adsorption isotherms for the adsorption of Ag(I) on the sample ES360: (a) Langmuir; (b) Freundlich.


z et al. / Chemosphere 146 (2016) 458e471

M. Bala

selecting different criteria, thus suggesting interesting conclusions.

They key data for these comparisons, being the zeta potential and
Qm values, are presented in Table 6 below.

3.5.1. Zeta potential of the two biomaterials

The zeta potential value for the ES360 in water is much less
negative than in the case of the ESM0 at the pH selected for the
adsorption. This is the result of smaller amount of charged groups
present on the surface of the ES. The values in the presence of silver(I) ions are also signicantly lower for the ES. The difference in
the zeta potential values in water and in silver(I) salt is signicantly
higher for the ESM, therefore predetermining it to be a better
adsorbent of the Ag(I) ions.
In the case of Cd(II) ions, the ZP value for the ESM is even more
positive than in the case of Ag(I). This phenomenon could be
possibly connected with the more positive charge of Cd(II) ion. The
ZP value for the ES360 was not recorded in the previous work and
therefore cannot be compared with the value of ESM0.

3.5.2. Non-treated adsorbents

The non-milled materials exhibit different afnity toward the
studied ions. In the work by Ho et al. (Ho et al., 2014) the values for
ES, ESM and the material composed of both these components were
compared with the result that the ESM is the best adsorbent. In the
present work, the maximum adsorption capacity 52.91 mg g1 for
the non-treated ESM is evidenced, whereas for the pre-milled ES
(ES0), the obtained qe value (as the Qm was not calculated) is
38.7 mg g1. It can be therefore concluded that ESM is a better
adsorbent for the Ag(I) ions than the ES, thus conrming the results
by Ho et al. It has to be stressed out, that ES0 sample used in the
present study was pre-milled and therefore cannot be considered
natural adsorbent. It is highly probable that the qe value of the
natural ES would be signicantly lower than the value of ES0.
Considering the adsorption of cadmium(II), the Qm value
23.419 mg g1 was evidenced for the ESM0. Koumanova et al.
(Koumanova et al., 2002) reported this value to be 24.27 mg g1, so
the results are very close. However as the Langmuir model does not
t well in either of these studies, it is probably better to consider
the value qe equal to 14.7 mg g1 in further comparisons. If the
Freundlich parameters are considered, Kf value 6.935 mmol g1 was
evidenced, whereas in Koumanova et al. (2002), it was signicantly
higher- 32.49 mol g1. However, in the present case we have reported almost ideal t of the Freundlich model for the adsorption of
the Cd(II) on the ESM, whereas in the paper (Koumanova et al.,
2002), R2 was only 0.85 and moreover, it has to be kept in mind,
that there are always some experimental differences when
comparing the values form different works, which could signicantly alter the results. If the above-mentioned qe value obtained
for the ESM is compared with the natural ES (in Flores-Cano et al.
(2013)) it was reported to be up to 4 mg g1), it can be concluded
that the natural ESM is a better adsorbent also for the Cd(II) ions.

Table 6
The zeta potential and Qm values for the studied adsorbents and ions.
Ion

e
Ag(I)
Cd(II)
a

Qm [mg.g1]

Zeta potential [mV]

ESM0

ES360

ESM0

ES360

31.5 (pH 6, Ag(I))

38.5 (pH 7, Cd(II))
17.9
43.3

11.3a

3.8a
e

52.910
23.419

55.7
488.82a

This value is taken from the paper (Bal

a
z et al., 2015a).

469

3.5.3. The effect of milling

It can be seen from the results that milling has a different impact
on both studied biomaterials. It was shown earlier in this paper that
it has more-or-less negative inuence on the ESM, however it
signicantly improves the adsorption ability of the ES. In the case of
Ag(I) adsorption, the qe value for the pre-milled ES is 38.7 mg g1,
and by the application of the long-term milling, it is possible to
increase its adsorption ability to more-or less the same level as it is
for the natural ESM (the value 55.7 mg g1 is evidenced for the
sample ES360). For the cadmium(II) adsorption, only slight premilling (sample ES0) turns the ES into better adsorbent than the
natural ESM (qe value 48.1 mg g1 was evidenced). The adsorption
ability becomes even more signicant as the milling time increases
(Bal

a
z et al., 2015a).
3.5.4. The afnity toward Ag(I) and Cd(II) ions
The two studied biomaterials seem to behave differently toward
the two ions. As can be seen from Table 2, the ESM exhibits almost
two-fold higher afnity toward Ag(I) in comparison with Cd(II) ion,
as is documented by the higher Qm and Kf values. As the atomic radii
of the two atoms are quite similar, the different behavior is probably connected with the charge of the ions. It seems that lower
charge seems to be more suitable for the ESM. This could be
possibly proved in the future by the experiments with the
adsorption of different metal(I) ions on the ESM.
As for the ES, we did not study the behavior of the natural
biomaterial. The pre-milled and milled ES were studied in detail.
The qe value for the ES0 sample is 38.7 mg g1 and 48.1 mg g1 for
the Ag(I) and Cd(II) ions, respectively, suggesting the higher afnity
of the ES toward Cd(II) ions. By the application of milling, this difference becomes even more signicant (see the values for the
ES360 sample in Table 4). The higher afnity of the ES toward Cd(II)
ions could possibly connected with the similarity in the charge
between the Ca(II) and Cd(II) ions, which could be possibly interchanged. However, this was studied in detail in other works (FloresCano et al., 2013; Bal

a
z et al., 2015a). There is one last phenomenon
to be discussed in the case of the milled ES in relation to the
adsorption ability toward Ag(I) and that is the calcite-aragonite
phase transformation occurring during milling. It was discussed
in detail in relation to the adsorption of Cd(II) ions in our recent


work (Bala
z et al., 2015a). According to the paper (Demina et al.,
2012), it seems that the aragonite phase exhibits higher afnity
toward Cd(II) than toward Ag(I), which is conrmed also in this
study for the milled ES (sample ES360 contains 54% aragonite)
(Bal

a
z et al., 2015a).
4. Conclusions
In the present paper, the adsorption behavior of both components of the eggshell waste, namely the eggshell (ES) and the
eggshell membrane (ESM) was compared with the focus on the
inuence of milling.
Firstly, mild milling was applied on the ESM, in order to partly
maintain its brous structure with the aim to potentially increase
its application potential. No changes were observed in the infrared
spectra after milling, being the proof that no chemical changes
occurred within the process. The values of the specic surface area
decreased dramatically in the rst 5 min of milling, while further
milling brought about only a slight decrease, thus documenting the
gradual deterioration of the brous structure. The SEM images of
the ESM milled for 30 min showed the two types of morphology
(the residues of the bers at the surface layer and more-or-less
maintained brous structure in the bulk layer).
The adsorption ability of the ESM toward cadmium(II), silver(I)
and zinc(II) ions was also investigated. According to zeta potential

470

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M. Bala

measurements, the optimum pH for the adsorption of Ag(I), Cd(II)

and Zn(II) ions were 6, 7 and 7, respectively. The ESM exhibited a
selectivity toward different ions. The zinc(II) ions were not adsorbed at all. The cadmium(II) ions were adsorbed to small extent and
the afnity of the ESM toward silver(I) ions was by far the highest. It
was shown that milling did not bring about any improvement in
the adsorption ability of the ESM. The adsorption of Cd(II) and Ag(I)
on the ESM was evaluated using the Langmuir and Freundlich
models. Whereas the former one was more suitable for the
adsorption of Ag(I), the latter for Cd(II), thus suggesting different
mechanisms of adsorption. The calculated value of the maximum
adsorption capacity according to Langmuir model was 52.9 and
23.4 mg g1 for Ag(I) and Cd(II) ions, respectively. The presence of
both adsorbed species on the ESM was conrmed by elemental
mapping and EDX measurements. The desorption experiments
have shown the difference in the stability of the Ag- and Cd-laden
ESM. Although both ions slowly leak into the distilled water, the
process is more pronounced for Cd(II), thus conrming the potentially lower share of the irreversible adsorption, compared to Ag(I).
The adsorption of Ag(I) ions was tested also on the ES. The zeta
potential measurements revealed that the ideal pH for the
adsorption tests was 5. On the contrary to the ESM, milling brought
about the increase of the adsorption ability of the ES toward Ag(I)
ions, although 60 min of milling was not enough. However when
the duration of milling was extended to 360 min, the adsorption
ability was increased signicantly. This is most probably connected
with the large amount of aragonite phase in the system. The
Langmuir model was proved to be suitable to describe the
adsorption process and the Qm value 55.7 mg g1 was calculated.
The possibility of applying milled ES in technology was demonstrated on the adsorption of silver(I) from the technological waste,
where almost half of silver(I) ions were successfully adsorbed on
the ES.
In the last part, various comparisons were outlined with the
general conclusion that the eggshell biomaterial is very interesting
in the terms of the selectivity. Whereas the ESM exhibits higher
afnity toward Ag(I) ions, the situation is the other way round in
the case of the ES. The milling makes the ES more efcient adsorbent than the ESM, favoring the adsorption of Cd(II) over Ag(I) ions.
In general, the obtained results, namely the Qm values obtained
for the adsorption of Ag(I) ions are comparable to many other
natural or modied biosorbents. We tried to show within this work,
that the eggshell waste is very interesting for the potential applications for the wastewater treatment and is worth much more than
just a space in the trash can.
Acknowledgments
This work was supported by the Slovak Research and Development Agency under the contract No. APVV-14-0103. The support of
other projects, namely Centre of Excellence of Slovak Academy of
Sciences (project CFNT-MVEP), Slovak Grant Agency VEGA (projects
2/0027/14, 2/0051/14 and 2/0097/13) and European Regional
Development Fund (projects nanoCEXmat I (ITMS 26220120019)
and nanoCEXmat II (ITMS 26220120035)) is also gratefully
acknowledged.
References
Ahmad, M., Usman, A.R.A., Lee, S.S., Kim, S.C., Joo, J.H., Yang, J.E., Ok, Y.S., 2012.
Eggshell and coral wastes as low cost sorbents for the removal of Pb2, Cd2
and Cu2 from aqueous solutions. J. Ind. Eng. Chem. 18, 198e204.
Arami, M., Limaee, N.Y., Mahmoodi, N.M., 2006. Investigation on the adsorption
capability of egg shell membrane towards model textile dyes. Chemosphere 65,
1999e2008.


Bala
z, P., 2000. Extractive Metallurgy of Activated Minerals. Elsevier, Amsterdam.


Bala
z, P., 2008. Mechanochemistry in Nanoscience and Minerals Engineering.
Springer, Berlin Heidelberg.
Bal

a
z, M., 2014. Eggshell membrane biomaterial as a platform for the applications in
materials science. Acta Biomater. 10, 3827e3843.

s, M.J., Zorkovska

, A., 2013a. Bio-inspired mechanoBal

a
z, M., Bal

a
z, P., Sayague
chemical synthesis of semiconductor nanomaterial using eggshell membrane.
Mater. Sci. Semicond. Process. 16, 1899e1903.

, M., Bala


Bal

a
z, P., Achimovi
cova
z, M., Billik, P., Cherkezova-Zheleva, Z., Criado, J.M.,

, E., Gaffet, E., Gotor, F.J., Kumar, R., Mitov, I., Rojac, T.,
Delogu, F., Dutkova
Senna, M., Streletskii, A., Wieczorek-Ciurowa, K., 2013b. Hallmarks of mechanochemistry: from nanoparticles to technology. Chem. Soc. Rev. 42, 7571e7637.

, A., Bala


Bal

a
z, P., Calka, A., Zorkovska
z, M., 2013c. Processing of eggshell biomaterial
by electrical discharge assisted mechanical milling (EDAMM) and high energy
milling (HEM) techniques. Mater. Manuf. Process. 28, 343e347.
a

kova

, Z., Bal

Bal

a
z, M., Bujn
a
z, P., Zorkovsk

a, A., Dankov

a, Z., Brian
cin, J., 2015a.
Adsorption of cadmium(II) on waste biomaterial. J. Colloid Interface Sci. 454,
121e133.



, A., Fabia

n, M., Girman, V., Brian
Bala
z, M., Zorkovska
cin, J., 2015b. Eggshell biomaterial: characterization of nanophase and polymorphs after mechanical activation. Adv. Powder Technol. 26, http://dx.doi.org/10.1016/j.apt.2015.1009.1003,
1597e1608.
Bandekar, J., 1992. Amide modes and protein conformation. Biochim. Biophys. Acta
1120, 123e143.
Barakat, M.A., 2011. New trends in removing heavy metals from industrial wastewater. Arab. J. Chem. 4, 361e377.
Bernhoft, R.A., 2013. Cadmium toxicity and treatment. Article ID 394652 Sci. World
J. 2013, 1e7.
a

kova

, Z., Bala



, A., Sayague

s, M.J., Kova


Bujn
z, P., Zorkovska
c, J., Timko, M., 2013.
Arsenic sorption by nanocrystalline magnetite: an example of environmentally
promising interface with geosphere. J. Hazard. Mater. 262, 1204e1212.
Butyagin, P.Y., 1989. Active States in Mechanochemical Reactions. Harwood Academic Publishers, Reading.
Chen, J.P., 2010. Decontamination of Heavy Metals: Processes, Mechanisms and
Applications. CRC Press, Taylor & Francis Group, Boca Raton.
Cheng, X.Z., Liu, J., Zou, S.F., Cheng, K., 2011a. Monitoring of heavy metal cadmium in
environmental water sample by eggshell membrane preconcentration coupled
with GF-AAS. In: 2011 International Conference on Electric Technology and Civil
Engineering (ICETCE 2011) e Proceedings, pp. 1356e1359.
Cheng, X.Z., Shao, K., Shen, S.Y., Hu, S.H., Qiu, H.O., 2011b. Determination of trace
silver in polymetallic ore samples by ame atomic absorption spectrometry
after solid-phase extraction using a microcolumn comprising eggshell membrane. Geostand. Geoanal. Res. 35, 461e469.
Coruh, S., Senel, G., Ergun, O.N., 2010. A comparison of the properties of natural
clinoptilolites and their ion-exchange capacities for silver removal. J. Hazard.
Mater. 180, 486e492.
Daraei, H., Mittal, A., Mittal, J., Kamali, H., 2013. Optimization of Cr(VI) removal onto
biosorbent eggshell membrane: experimental & theoretical approaches.
Desalin. Water Treat. 52, 1307e1315.
Daraei, H., Mittal, A., Noorisepehr, M., Mittal, J., 2015. Separation of chromium from
water samples using eggshell powder as a low-cost sorbent: kinetic and thermodynamic studies. Desalin. Water Treat. 53, 214e220.
de Paula, H.A., Becker, J.G., Davis, A.P., 2008. Characterization of the uptake of
divalent metal ions by a hatchery residual. Environ. Eng. Sci. 25, 737e746.
Demina, L.L., Galkin, S.V., Dara, O.M., 2012. Trace metal bioaccumulation in the
shells of mussels and clams at deep-sea hydrothermal vent elds. Geochem. Int.
50, 133e147.
Demirbas, A., 2008. Heavy metal adsorption onto agro-based waste materials: a
review. J. Hazard. Mater. 157, 220e229.
Dong, Q., Su, H.L., Zhang, D., Cao, W., Wang, N., 2007. Biogenic synthesis of tubular
SnO2 with hierarchical intertextures by an aqueous technique involving
glycoprotein. Langmuir 23, 8108e8113.
Flores-Cano, J.V., Leyva-Ramos, R., Mendoza-Barron, J., Guerrero-Coronado, R.M.,
Aragon-Pina, A., Labrada-Delgado, G.J., 2013. Sorption mechanism of Cd(II) from
water solution onto chicken eggshell. Appl. Surf. Sci. 276, 682e690.
Fu, F.L., Wang, Q., 2011. Removal of heavy metal ions from wastewaters: a review.
J. Environ. Manag. 92, 407e418.

ber, F., Luk


th, A.L., Horva

th, Z.E., Miha

ly, J., Bal

Gergely, G., We
acs, I., To
azsi, C., 2010.
Preparation and characterization of hydroxyapatite from eggshell. Ceram. Int.
36, 803e806.
Ghani, S.A., Young, H.C., 2010. Conductive polymer based on polyaniline-eggshell
powder (PANI-ESP) composites. J. Phys. Sci. 21, 81e97.
Godt, J., Scheidig, F., Grosse-Siestrup, C., Esche, V., Brandenburg, P., Reich, A.,
Groneberg, D.A., 2006. The toxicity of cadmium and resulting hazards for human health. J. Occup. Med. Toxicol. 1, 1e6.
Gunasekaran, S., Sailatha, E., 2008. Vibrational analysis of pyrazinamide. Indian J.
Pure Appl. Phys. 46, 315e320.
Hambidge, K.M., Krebs, N.F., 2007. Zinc deciency: a special challenge. J. Nutr. 137,
1101e1105.
Hincke, M., Gautron, J., Nys, Y., Rodriguez-Navarro, A.B., McKee, M.D., 2011. The
eggshell: structure and protective function. In: Nys, Y., Bain, M., Van
Immerseel, F. (Eds.), Improving the Safety and Quality of Eggs and Egg Products,
Egg Chemistry, Production and Consumption, vol. 1. Woodhead Publishing in
Food Science, Technology and Nutrition, Cambridge, pp. 151e182.
Ho, J.H., Yeh, Y.N., Wang, H.W., Khoo, S.K., Chen, Y.H., Chow, C.F., 2014. Removal of
Nickel and silver ions using eggshells with membrane, eggshell membrane, and


z et al. / Chemosphere 146 (2016) 458e471

M. Bala
eggshells. Food Sci. Technol. Res. 20, 337e343.
Ishikawa, S., Suyama, K., Arihara, K., Itoh, M., 2002. Uptake and recovery of gold ions
from electroplating wastes using eggshell membrane. Bioresour. Technol. 81,
201e206.
Janusz, W., Khalameida, S., Sydorchuk, V., Skwarek, E., Zazhigalov, V., SkubiszewskaZieba, J., Leboda, R., 2010. Some properties of milled vanadium phosphates.
Adsorpt. J. Int. Adsorpt. Soc. 16, 333e341.
Kaiden, K., Matsui, T., Tanaka, S., 1987. A study of the amide-III band by FT-IR
spectrometry of the secondary structure of albumin, myoglobin, and gammaglobulin. Appl. Spectrosc. 41, 180e184.
Kong, J., Yu, S., 2007. Fourier transform infrared spectroscopic analysis of protein
secondary structures. Acta Biochem. Biophys. Sin. 39, 549e559.
Koumanova, B., Peeva, P., Allen, S.J., Gallagher, K.A., Healy, M.G., 2002. Biosorption
from aqueous solutions by eggshell membranes and Rhizopus oryzae: equilibrium and kinetic studies. J. Chem. Technol. Biotechnol. 77, 539e545.
Kuh, S.E., Kim, D.S., 2000. Removal characteristics of cadmium ion by waste egg
shell. Environ. Technol. 21, 883e890.
Kumaraswamy, K., Dhananjaneyulu, B.V., Cijetha, P., Prasanna Kumar, Y., 2015. Kinetic and equilibrium studies for the removal of chromium using eggshell
powder. Res. J. Pharm. Biol. Chem. Sci. 6, 529e536.
Lata, S., Singh, P.K., Samadder, S.R., 2015. Regeneration of adsorbents and recovery
of heavy metals: a review. Int. J. Environ. Sci. Technol. 12, 1461e1478.
Leyva-Ramos, R., Landin-Rodriguez, L.E., Leyva-Ramos, S., Medellin-Castillo, N.A.,
2012. Modication of corncob with citric acid to enhance its capacity for
adsorbing cadmium(II) from water solution. Chem. Eng. J. 180, 113e120.
Li, B.X., Lan, D., Zhang, Z.J., 2008. Chemiluminescence ow-through biosensor for
glucose with eggshell membrane as enzyme immobilization platform. Anal.
Biochem. 374, 64e70.
Lihareva, N., Tzvetanova, Y., Petrov, O., Dimova, L., 2013. Sorption of silver cations by
natural and Na-exchanged mordenite. Sep. Sci. Technol. 48, 617e625.
Liu, D., Li, Y.G., Xu, H., Sun, S.Q., Wang, Z.T., 2008. Differentiation of the root of
cultivated ginseng, mountain cultivated ginseng and mountain wild ginseng
using FT-IR and two-dimensional correlation IR spectroscopy. J. Mol. Struct. 883,
228e235.
Mack, C.L., Wilhelmi, B., Duncan, J.R., Burgess, J.E., 2007. Biosorption of precious
metals. Biotechnol. Adv. 25, 264e271.
Mohammadi, M., Lahijani, P., Mohamed, A.R., 2014. Refractory dopant-incorporated
CaO from waste eggshell as sustainable sorbent for CO2 capture: experimental
and kinetic studies. Chem. Eng. J. 243, 455e464.
Montinaro, S., Concas, A., Pisu, M., Cao, G., 2007. Remediation of heavy metals
contaminated soils by ball milling. Chemosphere 67, 631e639.
Naito, W., Kamo, M., Tsushima, K., Iwasaki, Y., 2010. Exposure and risk assessment of
zinc in Japanese surface waters. Sci. Total Environ. 408, 4271e4284.
Nys, Y., Gautron, J., Garcia-Ruiz, J.M., Hincke, M.T., 2004. Avian eggshell mineralization: biochemical and functional characterization of matrix proteins. C. R.
Palevol 3, 549e562.


, A., Skvarla,
Orolinov

a, Z., Mockov
ciakova
J., 2010. Sorption of cadmium (II) from
aqueous solution by magnetic clay composite. Desalin. Water Treat. 24, 284e292.
Park, H.J., Jeong, S.W., Yang, J.K., Kim, B.G., Lee, S.M., 2007. Removal of heavy metals
using waste eggshell. J. Environ. Sci. China 19, 1436e1441.
Rath, M.K., Choi, B.H., Ji, M.J., Lee, K.T., 2014. Eggshell-membrane-templated synthesis of hierarchically-ordered NiO-Ce0.8Gd0.2O1.9 composite powders and

471

their electrochemical performances as SOFC anodes. Ceram. Int. 40,

3295e3304.
Rosenman, K.D., Moss, A., Kon, S., 1979. Argyria: clinical applications of exposure to
silver nitrate and silver oxide. J. Occup. Med. 21, 430e435.
Rosenman, K.D., Seixas, N., Jacobs, I., 1987. Potential nephrotoxic effects of exposure
to silver. Br. J. Ind. Med. 44, 267e272.
Sari, A., Tuzen, M., 2013. Adsorption of silver from aqueous solution onto raw
vermiculite and manganese oxide-modied vermiculite. Microporous Mesoporous Mater. 170, 155e163.
hl, D.F., Steinhoff, D., 1960. Experimental carcinogenesis in rats with colloidal
Schma
silver and gold solutions. Z. Krebsrforsch 63, 586e591.
Shaheen, S.M., Eissa, F.I., Ghanem, K.M., Gamal El-Din, H.M., Al Anany, F.S., 2013.
Heavy metals removal from aqueous solutions and wastewaters by using
various byproducts. J. Environ. Manag. 128, 514e521.
Shimada, Y., Niide, T., Kubota, F., Kamiya, N., Goto, M., 2010. Selective separation
of precious metals using biomass materials. Kagaku Kogaku Ronbun 36,
255e258.
Stadelman, W.J., 2000. Egg and egg products. In: Francis, F.J. (Ed.), Encyclopedia of
Food Science and Technology. John Wiley & Sons, New York, pp. 593e599.
Su, H.L., Han, J., Wang, N., Dong, Q., Zhang, D., Zhang, C.F., 2008. In situ synthesis of
lead sulde nanoclusters on eggshell membrane bers by an ambient bioinspired technique. Smart Mater. Struct. 17.
Suresh, C., Reddy, D.H.K., Harinath, Y., Naik, B.R., Seshaiah, K., Reddy, A.V.R., 2014.
Development of wood apple shell (Feronia acidissima) powder biosorbent and
its application for the removal of Cd(II) from aqueous solution. Article ID
154809 Sci. World J. 2014.
Suyama, K., Fukazawa, Y., Umetsu, Y., 1994. A new biomaterial, hen egg-shell
membrane, to eliminate heavy-metal ion from their dilute waste solution.
Appl. Biochem. Biotechnol. 45e46, 871e879.
Sydorchuk, V., Khalameida, S., Zazhigalov, V., Skubiszewska-Zieba, J., Leboda, R.,
Wieczorek-Ciurowa, K., 2010. Inuence of mechanochemical activation in
various media on structure of porous and non-porous silicas. Appl. Surf. Sci. 257,
446e450.
Tsai, W.-T., Yang, J.-M., Hsu, H.-C., Lin, C.-M., Lin, K.-Y., Chiu, C.-H., 2008. Development and characterization of mesoporosity in eggshell ground by planetary ball
milling. Microporous Mesoporous Mater. 111, 379e386.
Veglio, F., Beolchini, F., 1997. Removal of metals by biosorption: a review. Hydrometallurgy 44, 301e316.
Wang, S., Wei, M.H., Huang, Y.M., 2013. Biosorption of multifold toxic heavy metal
ions from aqueous water onto food residue eggshell membrane functionalized
with ammonium thioglycolate. J. Agric. Food Chem. 61, 4988e4996.
Weymuth, T., Jacob, C.R., Reiher, M., 2010. A local-mode model for understanding
the dependence of the extended amide III vibrations on protein secondary
structure. J. Phys. Chem. B 114, 10649e10660.
Whitehead, K.A., Benson, P.S., Verran, J., 2011. The detection of food soils on
stainless steel using energy dispersive X-ray and Fourier transform infrared
spectroscopy. Biofouling 27, 907e917.
Yao, Z.T., Chen, T., Li, H.Y., Xia, M.S., Ye, Y., Zheng, H., 2013. Preparation, characterization, and antibacterial activity of shell waste loaded with silver. J. Mater. Sci.
48, 8580e8587.
Zhao, Y.H., Chi, Y.J., 2009. Characterization of collagen from eggshelll membrane.
Biotechnology 8, 254e258.