International Journal of Biological Macromolecules 151 (2020) 355–365

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International Journal of Biological Macromolecules

journal homepage: http://www.elsevier.com/locate/ijbiomac

Influence of chitosan and magnetic iron nanoparticles on chromium

adsorption behavior of natural clay: Adaptive neuro-fuzzy
inference modeling
Rauf Foroutan a, Seyed Jamaleddin Peighambardoust a, Reza Mohammadi b,⁎, Mohsen Omidvar c,
George A. Sorial d, Bahman Ramavandi e,f,⁎⁎
a
Faculty of Chemical and Petroleum Engineering, University of Tabriz, Tabriz 5166616471, Iran
b
Polymer Research Laboratory, Department of Organic and Biochemistry, Faculty of Chemistry, University of Tabriz, Tabriz, Iran
c
Department of Occupational Health Engineering, Faculty of Health and Nutrition, Bushehr University of Medical Sciences, Bushehr, Iran
d
Environmental Engineering Program, Department of Chemical and Environmental Engineering, College of Engineering and Applied Science, University of Cincinnati, Cincinnati, OH, 45221-0012,
USA
e
Department of Environmental Health Engineering, Faculty of Health and Nutrition, Bushehr University of Medical Sciences, Bushehr, Iran
f
Systems Environmental Health and Energy Research Center, The Persian Gulf Biomedical Sciences Research Institute, Bushehr University of Medical Sciences, Bushehr, Iran

a r t i c l e i n f o a b s t r a c t

Article history: In the current study, the influence of iron oxide nanoparticles and chitosan (CS) on the adsorption capacity of nat-
Received 25 January 2020 ural clay for chromium removal from aqueous media was explored. Clay-based adsorbents (clay, CS/Clay, Clay/
Received in revised form 15 February 2020 Fe3O4, and CS/Clay/Fe3O4) were manufactured and their physicochemical properties were identified. The effects
Accepted 18 February 2020
of operating factors on the adsorption efficiency were optimized. The results showed that the adsorption equilib-
Available online 19 February 2020
rium data for the clay, CS/Clay, and Clay/Fe3O4 corresponds to the Langmuir model, while for the CS/Clay/Fe3O4 is
Keywords:
consistent with the Freundlich model. The maximum adsorption capacity (qmax) of Cr(VI) using clay, CS/Clay,
Cr(VI) Clay/Fe3O4 and CS/Clay/Fe3O4 were 63.69 mg/g, 80.30 mg/g, 97.08 mg/g, and 117.64 mg/g, respectively. It was
Clay-based adsorbent showed that the addition of chitosan and Fe3O4 magnetic nanoparticles to the clay increases its adsorption capac-
Chitosan/Clay ity. The values of ΔG° and ΔH° parameter for Cr adsorption using adsorbents were negative, indicating that the
Chitosan/Clay/Fe3O4 removal process is spontaneous and exothermic. The kinetic behavior obeyed the pseudo-second-order model.
Leather factory The chromium removal process using all the adsorbents had a two-step mechanism. The wastewater of a leather
factory was effectively treated using clay based-adsorbents. Based on R2, MSE, SSE, and ARE values, good agree-
ment was observed between the ANFIS model and experimental outcomes.
© 2020 Elsevier B.V. All rights reserved.

1. Introduction and mercury [5,6]. Chromium is usually present in two forms of 3+

Irregular disposal of wastewater containing heavy metals can be ex-
tremely hazardous to ecosystems and human health [1,2]. Heavy
metals, including chromium, are continually introduced into the envi-
ronment through the discharge of industrial wastewater such as tan-
ning, mining, metalworking, nuclear power, iron and steel, energy and
fuel industries [3,4]. Chromium is the seventh most abundant element
on earth that has increased in aquatic and terrestrial ecosystems over
the past few decades due to human activities. It is the most toxic
metal known to humans and other organisms after lead, cadmium,
⁎ Corresponding author.
⁎⁎ Correspondence to: B. Ramavandi, Department of Environmental Health Engineering,
Faculty of Health and Nutrition, Bushehr University of Medical Sciences, Bushehr, Iran.
E-mail addresses: r.mohammadi@tabrizu.ac.ir (R. Mohammadi),
b.ramavandi@bpums.ac.ir (B. Ramavandi).
and chromium 6+, the hexavalent form of which is about 500 to 1000
times more soluble in aqueous and soil environments and thus, is
more toxic than the trivalent form [7,8]. Chromium (VI) can easily accu-
mulate in the liver, stomach, and kidneys [9,10]. So, it can cause serious
illnesses in the human body. It can also damage the cell integrity and
function [11].
Among the heavy metal removal techniques, the adsorption method
has attracted widespread attention because of its advantages such as
cost-effectiveness, simple, effective, efficient, low operating cost, and re-
versibility [12–14]. Various adsorbents such as activated carbon, clay,
agricultural wastes, and natural polysaccharides (cellulose, chitin, chito-
san, and their derivatives) have been used as adsorbents in wastewater
treatment. In addition to the environmental field, natural polysaccha-
rides are also used in many economical and medical fields because of
their unique structure and properties, safety, biocompatibility and bio-
degradability [15]. Chitosan is a natural polymer made from chitin

https://doi.org/10.1016/j.ijbiomac.2020.02.202
0141-8130/© 2020 Elsevier B.V. All rights reserved.
356 R. Foroutan et al. / International Journal of Biological Macromolecules 151 (2020) 355–365
deacetylation and is the second and most abundant biological macro-
molecule having a highly reactive hydroxyl (OH) and amino (NH2)
groups [16]. This polymer can be easily combined with vinyl hydrophilic
monomers, polymeric blending, and mixtures with other functional
groups through physical-chemical methods (link copolymerization) to
provide effective properties [17,18]. Chitosan has attracted widespread
attention for its benefits such as non-toxicity, biodegradability and anti-
microbial properties and has been used in a variety of fields (medicine,
pharmaceuticals, tissue engineering, and environment) [19].
Clay is another material that has been widely used as an important
sorbent in the removal of heavy metals because they are inexpensive,
abundant, and environmentally stable [10,20,21]. It is noteworthy that
despite these advantages, natural clay has limited applications due to
their low adsorption capacity [22,23]. One of the natural clay soils is
bentonite which is the main constituent of montmorillonite. Montmo-
rillonite has two layers of tetrahedral silica comprising an octagonal alu-
mina layer [24,25]. Bentonite has a layered structure by replacing Al3+
in tetrahedral layers instead of Si4+ and replacing Mg2+ and/or Fe3+
in octahedral layers with a negative surface charge instead of Al3+
[26]. Therefore, since bentonite is negatively charged, its modification
with compounds such as magnetic iron nanoparticles and chitosan
may be very useful for adsorption of negatively charged metals such
as chromium.
Artificial intelligence (AI) as the widespread division of computer
science dealt with constructing intelligent machines capable of car-
rying out tasks, typically involve human cleverness [27]. AI consists
of different modeling techniques such as artificial neural networks
(ANN), fuzzy inference system (FIS) modeling, and adaptive neuro-
fuzzy inference system (ANFIS) [27]. One of the robust techniques
to demonstrate and infer the input-output relationship in intricated
nonlinear systems is fuzzy modeling. A fuzzy inference system (FIS)
contains four principal components including fuzzifier, fuzzy rules
(If-Then rules), fuzzy inference engine, and defuzzifier [28]. ANN
mimics biological nervous processing. Some specifications of the
ANNs such as reliability, straightforwardness, robustness, and non-
linearity have been caused to resolve and simulate many of complex
engineering systems [29]. While the ANNs could learn from experi-
mental data to solve the intricated non–linear, multi-dimensional
functional relationships, the ANFIS can mix the learning effect of
the ANN and the reasoning effect of the FIS, to result in a more real-
istic result [30]. In fact, an ANFIS structure is a multilayer feed-
forward network, which is a fusion of two robust intelligent systems
(ANN & FIS) [31]. ANFIS combines the computational power of ANN
with the reasoning capability of FIS to analyze the complicated non-
linear systems [31].
Recently, ANFIS has been widely used as a useful modeling tech-
nique in the wide area of science especially in water and wastewater
treatment [28,30]. Mandal et al. used the ANFIS to predict the re-
moval efficiency of ZEDA hybrid material for purification of As(III)
and Cr(VI) from water [27]. In another study, the PCA, ANFIS, and
GA was applied to forecast and optimize the effectiveness of the
Pistacia khinjuk activated carbon for methylene blue adsorption
[28]. Briefly, a zero-order TSK fuzzy-model consists of 5 layers
(namely Fuzzification, Rule, Normalization, Defuzzification, and Out-
put layers) (Fig. S1).
The purpose of the present study was to investigate the effect of chi-
tosan and magnetic iron nanoparticles on the ability of natural clay to
adsorb Cr(VI). The effect of various parameters on adsorbents perfor-
mance was investigated. FT-IR, AFM, SEM, VSM, TEM, and XRD analyses
were applied to investigate the properties of the natural clay-based ad-
sorbents The kinetic and isotherm studies have also been carried out for
the process of adsorption of chromium (VI) using manufactured adsor-
bents and the ability of the adsorbents to purify a real effluent from in-
dustrial plants has also been explored. The ANFIS model was also used
to predict the adsorption efficiency of the 4 types of adsorbents with re-
gard to the process conditions.
2. Experimental
2.1. Chemicals and solutions
The natural clay used in this study was obtained from mines in
Dashtestan, Bushehr province, Iran. Chitosan (CS) with medium molec-
ular weight and a viscosity of 200-800cp was obtained from Sigma Al-
drich. Acetic acid, sodium hydroxide, hydrochloric acid, FeCl3.6H2O,
FeCl2 .4H2O and potassium dichromate (K2Cr2O7) were prepared and
used by the Merck Company. The chromium stock solution was pre-
pared from the dissolution of 2.828 g of potassium dichromate
(K2Cr2O7) in one liter of distilled water. In the adsorption process of
chromium (VI) using clay-based adsorbents, a 1 M solution of sodium
hydroxide or hydrochloric acid was used to adjust the solution's pH.
2.2. Preparation of clay-based adsorbents
2.2.1. Natural clay and CS/clay composite
Natural clay was first powdered using a mill, then graded using a
sieve No. 25 (ASTM E11) and used as the base material for the produc-
tion of the desired composites. In order to produce Chitosan/Clay com-
posite, 2 g of chitosan (CS) was dissolved in 100 mL of 1 M acetic acid
solution. Then, about 0.5 g of clay was added to the chitosan solution
and stirred using a magnetic stirrer for 2 h to completely dissolve the
clay in the chitosan solution and to obtain a uniform mixture. Sodium
hydroxide solution (3 mol/L) was added drop-wise to the CS/Clay mix-
ture after complete mixing of the clay in the chitosan solution and
stirred to complete the networking process using a magnetic stirrer.
The composite was rinsed with double distilled water to be thoroughly
neutralized (pH 6–7). The generated composite was incubated in the
oven for 24 h at 70 °C to dry and then the powder was used to uptake
Cr(VI).
2.2.2. Magnetic composites based on natural clay (clay/Fe3O4 and CS/clay/
Fe3O4)
The chemical deposition method was used to produce magnetic clay
composite. First, an aqueous solution containing a 1: 2 M ratio of Fe(III):
Fe(II) was prepared. Then, 1 g of natural clay was added and mixed for
20 min using ultrasonic. Upon completion of the desired time, the tem-
perature was raised to 85–90 °C and then the NaOH solution (3 M,
50 mL) was added drop-wise and mixed for 30 min. The generated mag-
netic composite was placed at ambient temperature and separated from
the aqueous solution using an external magnetic field (a simple mag-
net). Finally, the resulting composite was rinsed to neutralize and
then dried (105 °C for 24 h) and stored for use in the tests.
The chemical precipitation technique was also used to produce mag-
netic CS/Clay/Fe3O4 magnetic composite. Briefly, 2 g of chitosan (2% w/
v) was first added to 100 mL of 1 M acetic acid solution and stirred for
2 h until the chitosan was completely dissolved. Then, about 1 g of nat-
ural clay and 20 mL of Fe(III) and Fe(II) solution with the molar ratio of
1: 2 was slowly added to the chitosan solution at 80 °C and stirred for
20 min using a magnetic stirrer to allow the clay and iron ions to
completely dissolve in the chitosan solution. Then, 50 mL of sodium hy-
droxide solution (3 M) was added drop-wise and stirred using a mag-
netic stirrer for 50 min. The produced black precipitate containing
chitosan, natural clay, and magnetic iron nanoparticles was separated
and washed several times with distilled water to be completely neutral-
ized (pH 6–7). The manufactured composite was incubated in the oven
at 70 °C for 24 h to dry and then used as an adsorbent in the adsorption
process of Cr(VI).
2.3. Characteristics measurement of the adsorbents
The devices like FTIR (Broker victor 22), scanning electron micros-
copy (SEM-TESCAN MIRA3-FEG), LEO 906 transmission electron mi-
croscopy (TEM), atomic force microscopy (AFM) (NanoScope III,
 R. Foroutan et al. / International Journal of Biological Macromolecules 151 (2020) 355–365 357

Digital Instruments Co., USA) were used to characterize the clay based- procedure for analysis of the data using ANFIS can be briefly summa-
adsorbents. rized as follows:
Normalization of the inputs: Before the inputs fed to the network, the
2.4. Adsorption tests data were normalized using the following equation:

Chromium uptake experiments were performed in batch mode in X−X min

X norm ¼ −X min ð5Þ
200 mL-Erlenmeyer flasks. The effect of pH (2–8) on the Cr sorption ef- X max
ficiency was checked at the Cr concentration, adsorbent mass, and the
contact time of 10 mg/L, 1 g/L, 60 min, respectively. The maximum ad- where Xnorm, X, Xmin, and Xmax represent the normalized value, the vec-
sorption efficiency was reported as the optimum pH. After determining tor of values, the minimum value of the vector X, and the maximum
the optimum pH, the influence of time of contact (5–120 min), Cr con- value for the vector X, respectively.
centration (10–200 mg/L), temperature (25–50 °C), and adsorbent Selection of the training and validation variables: The data in the ANFIS
mass (0.5–4 g/L) on the removal efficiency at optimum pH was investi- were randomly split into two groups of training (70%) and checking
gated. Data obtained in the phase of the contact time effect were used to (30%).
conduct the kinetics of the Cr adsorption. All tests were done at 400 rpm Selection of membership functions (MFs): To develop the fuzzy infer-
in a shaker-incubator device (Parsazma Co., Iran). ence system (FIS) in ANFIS, the Gaussian form of MFs were selected as
After the desired time, depending on the type of adsorbents, an ex- the functions of the structure.
ternal magnetic field (magnet) or Whatman 42 filter paper was used !
to separate the reactants. The concentration of chromium (VI) was mea- ðx−cÞ2
f ðx; σ; cÞ ¼ exp − ð6Þ
sured by flame atomic absorption spectrometry method (Analytikjena, 2 σ2
Nova AA 400). The following equation was used to calculate the adsorp-
tion percentage (R%) and adsorption capacity of Cr(VI) at the desired Selection of the model for FIS generation: Because of the problem of
time (qt, mg/g) and equilibrium condition (qe, mg/g): “curse of dimensionality”, Genfis2 was used to generates the Sugeno-
type FIS using the subtractive clustering. The parameters of the Genfis2


½Cr initial −½Cr final left as the default values (range of influence of 0.5, the squash factor of
Rð%Þ ¼  100 ð1Þ
½Crinitial 1.25, the accept ratio of 0.5, the reject ratio of 0.15). To optimize the
ANFIS model, the hybrid method (a combination of least–squares esti-
½Crinitial −½Cr equilibria mation and backpropagation) was used. The number of epochs for the
qe ¼  Volume ð2Þ optimization were 30 epochs.
½adsorbentmass
Validation of the ANFIS: The mean–squared error (MSE), average rel-
ative error (ARE), the sum of squared errors (SSE), and coefficient of de-
½Crinitial −½Cr time
qt ¼  Volume ð3Þ termination (R2) were used to evaluate the performance of the ANFIS
½adsorbenmass
model.

It should be noted that adsorption experiments were performed  2 N

N
three times and the data is presented with standard deviation wherever Σi¼1 yprd;i −yexp;i  2
R2 ¼ 1− yprd;i −ym ð7Þ
needed in the figures. Σi¼1

2.5. Desorption and reuse study N 2

1
MSE ¼ Σi¼1 yprd;i −y exp;i ð8Þ
N
For desorption study, 1 g/L of adsorbents (natural clay, CS/Clay, Clay/
vffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
Fe3O4, and CS/Clay/Fe3O4 with 100 mL solution containing 10 mg/L Cr u  2
u N
(VI) was stirred under laboratory conditions such as optimum pH, reac- tΣi¼1 y exp;i −yprd;i
SSE ¼ ð9Þ
tion time of 50 min, and solution temperature of 25 °C. After each ad- N
sorption cycle, the adsorbents were removed from the solution and  
N 
rinsed twice with double distilled water to remove excess chromium 100 yprd;i −y exp;i 
ARE ¼ Σi¼1  % ð10Þ
ions precipitated on the adsorbent surface. The adsorbents were then N  y exp;i 
poured into 50 mL NaOH solution with different concentrations in the
range of 0.05–0.5 M and agitated for 120 min. After this time, the Cr con- where N is the number of experimental points, yprd,i is the predicted re-
centration in the filtrate was determined. The adsorption-desorption sponse, yexp,i is the experimental value, and ym is the mean value of the
experiment was carried out in 9 steps and the desorption and recyclabil- response.
ity of the adsorbents were evaluated. The Cr desorption (%) was com-
puted by the following formula [32]: 3. Results and discussion


The CrðVIÞ desorbed 3.1. Adsorbents characteristics
Desorption percentage ¼  100 ð4Þ
The CrðVIÞ adsorbed
FT-IR analysis results for pristine and used natural clay, CS/Clay,
Clay/Fe3O4, and CS/Clay/Fe3O4 are displayed in Fig. 1a,b. A wide absorp-
2.6. ANFIS model construction tion peak (from 3410 to 3429 cm−1) in the structure of the mentioned
adsorbents is due to the vibration of the -OH group [20,33,34]. Also, a
In this study, the ANFIS structure developed by considering the ad- low-intensity absorption peak at 2880–2921 cm−1 assigned to the C-
sorption process conditions (adsorbent dose, Cr concentration, pH, tem- H group [35,36]. In the natural clay structure, a series of weak and strong
perature, and contact time) as input variables. On the other hand, the absorption peaks were observed at 511–711 cm−1, 874 cm−1,
adsorption efficiency (%) was used as the output variable as this param- 1028 cm−1, and 1432 cm−1. These peaks can be due to the presence
eter is the most popular in the adsorption studies. Matlab R2015b script of Si-O-Si, Si-O-Al, and Si-O-Mg as well as bending vibrations of Si-O
was used to develop, train, and validate the network of ANFIS. The [37,38]. After the formation of CS/Clay, Clay/Fe3O4, and CS/clay/Fe3O4,
358 R. Foroutan et al. / International Journal of Biological Macromolecules 151 (2020) 355–365
Fig. 1. (a,b) FT-IR analyzes of clay, CS/Clay, Clay/Fe3O4, and CS/Clay/Fe3O4 before and after the Cr(VI) adsorption process, (c) VSM analysis for Fe3O4 nanoparticles and Clay/Fe3O4 and CS/
Clay/Fe3O4 composites, and (d) XRD analysis for Fe3O4 nanoparticles, Clay, CS/Clay, Clay/Fe3O4, and CS/Clay/Fe3O4.
the range of absorption peaks in the natural clay structure was changed.
These changes may reflect the interaction between chitosan molecules
and Fe3O4 magnetic nanoparticles with functional groups in the natural
clay. For example, in the natural clay structure, there is an absorption
peak at 1633 cm−1, which may be assigned to the -OH group. After
the generation of CS/Clay, Clay/Fe3O4, and CS/Clay/Fe3O4 composites,
the mentioned absorption peak (1633 cm−1) was shifted to
1613 cm−1, 1629 cm−1, and 1626 cm−1, respectively. This alteration
could be related to the interactions of the NH group and Fe3O4 nanopar-
ticles with the functional groups on the natural clay surface. Also, after
the formation of magnetic composites of Clay/Fe3O4 and CS/Clay/Fe3O4
new absorption peaks appeared at 543 cm−1 and 626 cm−1, respec-
tively, which could be due to Fe-O in the composite and confirm the
presence of Fe3O4 nanoparticles in the structure of the adsorbents
[39,40]. After chromium ion adsorption, the OH-functional group vibra-
tions in the structure of clay, CS/Clay, Clay/Fe3O4, and CS/Clay/Fe3O4
changed to 3415 cm−1, 3431 cm−1, 3341 cm−1, and 3406 cm−1, respec-
tively. This may be justified by the interaction between the OH-
functional group and the contaminant. It is also noteworthy that the
range of other absorption peaks such as Fe\\O, Si-O-Al, Si-O-Si, and Si-
O-Mg in the structure of the adsorbents has also changed after the chro-
mium sorption process. This can correspond to the vibrations and inter-
action between Cr\\O and/or Cr_O with the functional groups present
at the surface of the adsorbents [41]. Given the changes in the absorp-
tion peak range for the fresh and used adsorbents, it can be stated that
the adsorption of chromium ions from the aqueous solution using
clay, CS/Clay, Clay/Fe3O4, and CS/Clay/Fe3O4 is physically possible [42].
A vibrating sample magnetometer (VSM) was used to investigate
the magnetic behavior of Fe3O4 nanoparticles, Clay/Fe3O4, and CS/
Clay/Fe3O4 composites. The result of this test is shown in Fig. 1c. Accord-
ing to the result, the magnetic saturation values for Fe3O4 nanoparticles,
Clay/Fe3O4, and CS/Clay/Fe3O4 were 84.356 emu/g, 47.628 emu/g, and
11.504 emu/g, respectively. As can be seen, the magnetization satura-
tion value for the Clay/Fe3O4 and CS/Clay/Fe3O4 composites is signifi-
cantly lower than for the Fe3O4 magnetic nanoparticles. The decrease
in magnetization saturation of Clay/Fe3O4 and CS/Clay/Fe3O4 compos-
ites compared to Fe3O4 magnetic nanoparticles can be due to various
reasons like adsorbents size, the density of oxygen molecule (O2)
absorbed on the composite particles [33,43]. Therefore, given the mag-
netization parameter value as well as S-formed diagrams for the sam-
ples of Fe3O4 nanoparticles, Clay/Fe3O4, and CS/Clay/Fe3O4, it can be
concluded that the samples have the magnetic property and by using
an external magnetic field they can be separated from the solution,
which is one of the prominent advantages in the Cr adsorption process.
XRD analysis in the range 2θ equals 5–80° was used to study the
structure and properties of the adsorbents. The findings are illustrated
in Fig. 1d. The peaks observed in the XRD pattern of pure Fe3O4 nanopar-
ticles at 2θ (°) diffraction angles of 18.28, 30.14, 35.43, 43.1, 53.47, 56.98,
and 63.04 are confirming the crystalline structure of (111), (220), (311),
(400), (442), (511), and (440), respectively. The results also showed
that the magnetic Fe3O4 nanoparticles have a cubic inverse spinel struc-
ture [21,44]. Based on the results, there are peaks with different intensi-
ties in the natural clay structure which mainly related to quartz (SiO2),
diaspore (AlOOH), muscovite, and hematite (Fe2O3) [45]. Peaks tracked
 R. Foroutan et al. / International Journal of Biological Macromolecules 151 (2020) 355–365
at the 2θ (°) angles of 23.22, 25.64, 31.23, 37.27, 47.65, 50.24, 61.42, and
64.72 in natural clay have corresponded to calcite (CaCO3), quartz
(SiO2), montmorillonite [(Na,Ca)0.33(Al,Mg)2(Si4O10)(OH)2·nH2O],
muscovite [KAl2(AlSi3O10)(F,OH)2], muscovite, quartz, calcite (CaCO3),
and montmorillonite, respectively [46]. A series of peaks were observed
in the structure of these composites following the formation of Clay/
Fe3O4 and CS/Clay/Fe3O4, which corresponds to the crystalline surfaces
of (111), (220), (311), (400), (442), (511), and (440) [47]. This indicates
that Fe3O4 nanoparticles successfully composited in the structure of
produced adsorbents. Further, the studied materials (natural clay, CS/
Clay, Clay/Fe3O4, and CS/Clay/Fe3O4) have a crystalline structure.
The results of the SEM analysis are depicted in Fig. 2. The surface of
the natural clay has various grooves and pores (Fig. 2a) that can be in-
volved in the Cr adsorption process. After the formation of the CS/Clay
composite, the pores and roughness on the clay surface are almost re-
moved and the produced composite has a smooth and layered surface
(Fig. 2c). This may be due to the penetration of chitosan chains between
the clay layers. After the formation of Clay/Fe3O4 (Fig. 2e) and CS/Clay/
Fe3O4 (Fig. 2g), small and spherical particles were observed on the
clay surface, which increased the roughness and pores on the clay sur-
face. Spherical particles formed on the surface of natural clay can be
due to the formation of Fe3O4 magnetic nanoparticles. After the adsorp-
tion process, significant changes in the adsorbent surface were moni-
tored, which could be due to the adsorption of chromium ions.
Fig. 2. SEM analyzes for (a) natural clay, (b) natural clay after adsorption of Cr(VI), (c) CS/Clay composite, (d) CS/Clay composite after adsorption Cr(VI), (e) Clay/Fe3O4, (f) Clay/Fe3O4 after
adsorption of Cr(VI), (g) CS/Clay/Fe3O4 and (h) CS/Clay/Fe3O4 after adsorption of Cr(VI).
359
Therefore, it can be stated that the manufactured adsorbents have a
suitable ability to adsorb Cr(VI) from aqueous solutions.
Fig. 3a shows the TEM image for the magnetic Fe3O4 nanoparticles,
whereby the nanoparticle morphology is approximately spherical
with the particle size b50 nm. So, the spherical particles present at the
Clay/Fe3O4 surface (Fig. 2e) and CS/Clay/Fe3O4 (Fig. 2g) can be attrib-
uted to Fe3O4 nanoparticles. The morphology of natural clay using
TEM analysis is shown in Fig. 3b, which confirms that the clay has a lay-
ered structure. After the formation of the Clay/Fe3O4 composite (Fig. 3c),
the magnetic nanoparticles of Fe3O4 are well dispersed on the surface of
the clay layers with spherical morphology. Dark areas were observed in
CS/Clay and CS/Clay/Fe3O4 between the chitosan layers. The dark areas
can be attributed to the magnetic Fe3O4 nanoparticles in the composite
structure. Therefore, according to the results, it can be concluded that
the desired composite production is successful and the Fe3O4 nanopar-
ticles and clay layers are well dispersed in the composite structure.
The results of the AFM analysis are shown in Fig. 4. This analysis
shows three-dimensional images for the surface of the sample, so it
is a suitable method for investigating surface morphology and deter-
mining surface roughness. According to the results, the adsorbents
used have roughness and pores with different sizes that can be effec-
tive in the adsorption process. Also, according to the results of AFM
analysis, the average roughness values for natural clay, CS/Clay,
Clay/Fe3O4, and CS/Clay/Fe3O4 samples were 79.891 nm, 7.324 nm,
360 R. Foroutan et al. / International Journal of Biological Macromolecules 151 (2020) 355–365

Fig. 3. TEM analysis for samples of (a) Fe3O4 magnetic nanoparticles, (b) clay, (c) Clay/Fe3O4, (d) CS/Clay, and (e) CS/Clay/Fe3O4.

42.723 nm, and 8.430 nm, respectively. This indicates that the natu- and iron nanoparticles on the surface of natural clay can affect the ef-
ral clay surface interacts well with magnetic Fe3O4 nanoparticles and ficiency and adsorption capacity since suitable active sites (hydroxyl,
chitosan, and the chitosan and iron nanoparticle chains are success- carboxyl, carbonyl, etc.) are provided for the adsorption of chromium
fully formed on the clay surface. The placement of chitosan chains ions [48–50].

Fig. 4. AFM analysis for samples of (a) natural clay, (b) CS/Clay, (c) Clay/Fe3O4, and (d) CS/Clay/Fe3O4.
 R. Foroutan et al. / International Journal of Biological Macromolecules 151 (2020) 355–365 361

3.2. Assessment the effects pH, contact time, adsorbent dose, and pollutant
concentration on Cr adsorption by clay-based adsorbents
The influence of pH on the Cr adsorption using natural clay, CS/Clay,
Clay/Fe3O4, and CS/Clay/Fe3O4 was investigated (Fig. 5a). The maximum
Cr-adsorption efficiency was determined using CS/Clay and CS/Clay/
Fe3O4 composite at pH 2 and for natural clay and Clay/Fe3O4 composite
at pH 3. Such findings have been reported in previous investigations
[51]. The findings show that by growing the solution pH from 2 to 8
the chromium adsorption using the produced adsorbents is significantly
reduced. At high pH, metal ions such as chromium (VI) precipitate in the
form of hydroxide and their concentration in the medium decreases,
which in turn reduces the adsorption efficiency [52]. In addition, the de-
crease in the adsorption efficiency of Cr(VI) with increasing initial pH
can be explained by the shift of the adsorbent surface charge from a pos-
itive value to a negative one. This phenomenon results in repulsive
forces between the sorbent and the Cr contaminant [53]. Another rea-
son for the decrease in adsorption efficiency of chromium (VI) at high
pH is the ionic form of chromium in the aqueous media. Hexavalent
chromium ion can produce various ions like dichromate (Cr2O2− 7 ),
hydrochromate (HCrO− 2−
7 ), H2CrO4 or chromate (CrO4 ) [53]. At the ini-
tial pH range of 2–6, chromium ions have two predominant forms of
HCrO− 2−
4 and Cr2O7 , which are converted to CrO4
2−
by increasing pH
[9]. At the initial pH of 2–3, the dominant form of chromium (VI) is
HCrO− 4 with low adsorption energy of −2.5 to −0.6 k·cal/mol [54]. It
is notable that the ionic size of HCrO− 3
4 (44 cm /mol) is less than
Cr2O2−7 (73 cm 3
/mol) [8]. Therefore, the smaller size of the ionic pollut-
ant can penetrate the adsorber more easily (because it needs less
energy).
The Cr(VI) adsorption efficiency was changed over time using clay
and clay-based composites (Fig. 5b). According to the results, the ad-
sorption of Cr(VI) has two steps and the first stage is faster than the sec-
ond., the high speed of the process in the first step is due to the
availability of sufficient surface area for metal ion adsorption and the
high number of active sites [55–57]. The slow rate of the adsorption
process in the second step could be justified by the saturation of the ad-
sorbent active sites or lack of access to the active sites. Therefore, the
equilibrium adsorption time of Cr(VI) using natural clay (92.75%), CS/
Clay (94.28%), Clay/Fe3O4 (95.48%), and CS/Clay/Fe3O4 (96.35%) was de-
termined 60 min, 50 min, 40 min, and 30 min, respectively.
The results of the effect of adsorbent dose on adsorption efficiency
are illustrated in Fig. 5c. According to the reported results, by increasing
the adsorbent dose, the chromium uptake increased. Increasing the ad-
sorbent concentration provides more surface area for chromium re-
moval [3,58]. The 2 g/L adsorbent mass was determined as the
optimal value for all adsorbents.
According to Fig. 5d, the adsorption capacity of chromium (VI) de-
creased with increasing adsorbent dose using the adsorbents used.
The high amount of adsorbent causes active and accessible sites for
metal ion uptake to increase. Since the metal ion concentration in the
aqueous solution is a given value, not all active sites in the adsorbent
will be served and some of them will not be saturated. The reduction
in the total surface of the adsorbents, the reduction in the number of ac-
tive sites, and an increase in the metal ion penetration pathway in the
adsorbent [32,59].
The effect of the initial concentration of Cr(VI) on its uptake using
the adsorbents is supplied in the Supplementary Information (Fig. S2).
The results show that by rising the initial concentration of Cr(VI), the
adsorption efficiency using natural clay, CS/Clay, Clay/Fe3O4, and CS/
Clay/Fe3O4 decreased. This issue can explain by the rapid saturation of
the active sites in the adsorbents, causing all metal ions to not be
absorbed by the adsorbent [46,60]. In addition to saturating the adsor-
bent surface, another factor that can decrease the adsorption efficiency
by increasing the concentration of Cr(VI) is the negative electrostatic
force created at the adsorbent surface by the ions present in the aqueous
solution. When the chromium ions are placed on the adsorber surface,
the amount of negative charge on the surface of the adsorbent increases
and due to the homogenous charge between the surface of the adsor-
bent and the metal ion present in the aqueous solution, a repulsive
force is created between them. Thus, the adsorption rate is reduced.

100 100
(a) (b)
90
90
80
Adsorption (%)

Adsorption (%)

70 80 Clay
Clay
60 CS/Clay
CS/Clay 70
50 Clay/Fe O
Clay/Fe O
60 CS/Clay/Fe O
40 CS/Clay/Fe O
30 50
1 2 3 4 5 6 7 8 9 0 20 40 60 80 100 120
pH Time (min)

100 20
(c) (d)
95
15 Clay
Adsorption (%)

90
CS/Clay
qe (mg/g)

85 Clay 10 Clay/Fe O
80 CS/Clay CS/Clay/Fe O
Clay/Fe O 5
75
CS/Clay/Fe O
70 0
0 1 2 3 4 0.5 0.75 1 1.5 2 3 4
Adsorbent dosage (g/L) Adsorbent dosage (g/L)

Fig. 5. (a) Effect of initial pH on adsorption efficiency (temperature: 25 °C, Cr(VI): 10 mg/L, adsorbent dose: 1 g/L, contact time: 60 min, mixing rate: 400 rpm), (b) effect of contact time on
adsorption efficiency (Optimum pH, temperature: 25 °C, Cr(VI): 10 mg/L, adsorbent dose: 1 g/L, mixing rate: 400 rpm), (c) and (d)Effect of adsorbent dose on adsorption process efficiency
and capacity (optimum pH, contact time: 50 min, Cr(VI): 10 mg/L, temperature: 25 °C, mixing speed: 400 rpm).
362 R. Foroutan et al. / International Journal of Biological Macromolecules 151 (2020) 355–365
3.3. Isotherm study
Three of the most famous models were used to describe the equilib-
rium adsorption of chromium onto clay-based adsorbents.
The linear relationship of the Langmuir equilibrium model is given
by the following formula:
Ce 1 Ce
¼ þ
qe kL C e qmax
where, qmax and kL are the values of capacity (mg/g) and energy (L/g) of
the adsorption process, respectively. The adsorption intensity (which
described by RL = 1/[1 + kLCo]) is derived from the Langmuir model
and used for describing the process. Based on the values of the RL the
process is categorized to unsatisfactory (RL less than unity), irreversible
(RL equal to zero), linear (RL equal to unity), and satisfactory (RL from 0
to 1), respectively.
The nonlinear relation of the Freundlich formula is as follows:
1
ln qe ¼ ln K F þ lnC e
n
KF and n denote the Freundlich model constants. If the n value is ob-
tained 1, N1, and b1, then the Cr removal by the clay-based adsorbents
would be linear, physical, and chemical, respectively.
The D-R isotherm model can be described by the following formula:
ln qe ¼ ln qm −βε2
where qm denotes the maximum amount of adsorption capacity by clay
based-adsorbents (mg/g), β denotes the activity factor which repre-
sents the free sorption energy (mol2/kJ2).), Ɛ denotes the Polanyi poten-
tial (ɛ = RTln(1 + 1 / Ce)), R denotes the global constant of gases (which
equal to 8.314 J/mol/K), T denotes the absolute temperature (Kelvin),
pffiffiffiffiffiffi
and E (=1/ 2β ) denotes the average amount of free process energy
(kJ/mol). The adsorption process would be physical and chemical if
the free process energy is 8–16 kJ/mol and 8 kJ/mol, respectively
[32,61].
The linear relationship of assessed models for the adsorption process
of Cr(VI) from aqueous media using natural clay, CS/Clay, Clay/Fe3O4,
and CS/Clay/Fe3O4 are shown in Fig. S2b,c, respectively. The parameters
determined for these models are listed in Table S1. According to the re-
sults, in the adsorption process of chromium ions by natural clay, CS/
Clay, and Clay/Fe3O4, the correlation coefficient (R2) value induced by
Langmuir is higher than the Freundlich model. Therefore, it can be con-
cluded that monolayer surfaces had more effect on the Cr(VI) adsorp-
tion process than the multilayer and heterogeneous surfaces, whereas,
in CS/Clay/Fe3O4, multilayer surfaces was more effective. The maximum
adsorption capacity of Cr(VI) using clay, CS/Clay, Clay/Fe3O4, and CS/
Clay/Fe3O4 were computed to be 63.69 mg/g, 81.30 mg/g, 97.08 mg/g,
and 117.64 mg/g, respectively. It shows that the Cr uptake capacity of
Fig. 6. (a) Pseudo-first-order, (b) pseudo-second-order, and (C) intra-particle diffusion model for Cr(VI) adsorption process.
the produced composites is higher than that of simple clay. Considering
the RL and n parameters obtained from Langmuir and Freundlich equi-
librium models, it is implied that the adsorption process of Cr(VI)
using the clay-based adsorbents is physically desirable because the RL
values are between 0 and 1 and the n value is N1.
3.4. Kinetic study
ð11Þ
The kinetic of the chromium adsorption process was tested by using
the pseudo-first-order kinetic (PFOK), pseudo-second-order kinetic
(PSOK), and intra-particle diffusion (I-P-D) models.
The linear formulas of the PFOK and PSOK model are described as
follow:
PFOK : ln ðqe −qt Þ ¼ ln qe:cal −k1 t ð14Þ
t 1 t
PSOK : ¼ þ ð15Þ
qt k2 q2e qe:cal
ð12Þ where k1 (1/min) and k2 (g/mg·min) denote the kinetic rate
constants.
The graphs for PFOK and PSOK models and the corresponding pa-
rameter values are shown in Fig. 6a,b and Table S2, respectively. The ad-
sorption of chromium ions using different adsorbents follows the PSOK
model. According to the kinetic data reported in Table S2, for all the ad-
sorbents used, the R2 value for the PSOK model is higher than for that of
ð13Þ other models. Therefore, it can be implied that the kinetic performance
of the Cr(VI) adsorption from the liquid environment using different ad-
sorbents follows the PSOK model.
The linear relationship for the I-P-D model is as follows:
qt ¼ K i t 0:5 þ C ð16Þ
where Ki (mg/g·min0.5) denotes the I-P-D rate constant and the C pa-
rameter gives an estimate of the width of the boundary layer.
Fig. 6c shows the linear relationship of the I-P-D for the chromium
adsorption process using the desired adsorbents. According to the re-
sults, the kinetic data of the adsorption process is not linear and the ad-
sorption process is performed in two steps. The data set in Table S2
shows that the value of the Ki parameter in the first step is higher
than in the second one. The second step of the adsorption process is car-
ried out at a very slow rate where the penetration into the particle is
rate-limiting. Also, the results show that the C parameter in the second
stage is higher than the first one, indicating that for the second step the
boundary layer thickness has a more effect on the adsorption process.
3.5. Thermodynamic study
The entropy (ΔS°), enthalpy (ΔH°), and Gibbs free energy (ΔG°)
were calculated to assess the adsorption thermodynamics. The amount
 R. Foroutan et al. / International Journal of Biological Macromolecules 151 (2020) 355–365 363

Table 1 (98.64%), and CS/Clay/Fe3O4 (98.76%) occurred at 0.5 M sodium hydrox-

Characteristics of the leather factory wastewater before and after cleaning with clay-based ide solution.
adsorbents.
Fig. S5 shows the ability to reuse natural clay, CS/Clay, Clay/Fe3O4,
Characteristics Unit Fresh Treated by and CS/Clay/Fe3O4 adsorbents after the 9-step recovery process. The re-
Clay CS/Clay Clay/Fe3O4 CS/Clay/Fe3O4 sults demonstrate that the ability of adsorbents for Cr(VI) removal de-
creased with expanding reuse steps. This could be justified by the
As(V) mg/L 9.35 4.74 3.26 2.84 2.26
As(III) mg/L 12.73 6.48 4.38 3.72 3.15 saturation of active sites and also damage to the active sites of the adsor-
Cr(VI) mg/L 11.56 4.74 3.37 2.43 1.83 bents. The adsorption efficiency of the adsorbents up to the first 4 steps
BOD5 mg/L 153.27 140.32 132.27 127.68 124.55 of the adsorption-desorption process is N90%, indicating that the pro-
COD mg/L 308.37 298.51 283.34 274.64 268.45 duced adsorbents have a good ability to adsorb Cr(VI) from the aqueous
pH _____ 6.35 6.76 7.12 7.46 6.93
solution.

of Gibbs free energy is determined by the following formula: 3.7. Cleaning of real wastewater samples

ΔGo ¼ −RT ln ð1000  K D Þ
where KD (qe/Ce) denotes the equilibrium constant. The slope and inter-
cept of the Van't Hoff's equation are used to determine the enthalpy and
entropy parameters, respectively [23,62,63]. The linear relationship of
the Van't Hoff's equation is depicted in Fig. S3. The enthalpy and entropy
values are listed in Table S3. The linear equation of the model Van't
Hoff's is as follows:
ð17Þ To investigate the field ability of natural clay, CS/Clay, Clay/Fe3O4,
and CS/Clay/Fe3O4, the wastewater of a leather factory was treated.
The results are shown in Table 1. According to results, the real wastewa-
ter sample had a low organic matter and high heavy metal content. After
purification of the actual wastewater, the BOD5 and COD parameters, as
well as the content of heavy metals, decreased, indicating that the ad-
sorbents have a good ability to remove the contaminants from the
wastewater.

−ΔHo ΔSo 3.8. ANFIS results

ln ð1000  K D Þ ¼ þ ð18Þ
RT R
The results showed that the Gibbs free energy for chromium adsorp-
tion from the aqueous solution using all adsorbents has a negative value
which can be concluded that the process is performed spontaneously. It
should be noted that as the temperature increases, the Gibbs free energy
becomes more positive, indicating that the increase in temperature is an
inappropriate factor for the chromium adsorption and reduces the
spontaneous rate of the process. The enthalpy parameter also has a neg-
ative value for the adsorption of chromium by the studied adsorbents,
confirming that the adsorption process is exothermic.
3.6. Co-existing ions effects and adsorption-desorption study
Water and wastewater usually have different anions that can inter-
fere with the adsorption process. The effect of different anions (PO3−4 ,
− −
SO2−
4 , Cl , and NO3 ) on the adsorption efficiency of Cr(VI) was tested.
As depicted in Fig. S4, the adsorption efficiency of Cr(VI) is decreased
when the anions are present in the aqueous solution. It is noteworthy
−
that SO2−
4 and NO3 anions decrease the adsorption process efficiency
more than other anions. The anions present in the aqueous media con-
test with the Cr(VI) for positioning on the active sites resulting in re-
duced efficiency. The result is consistent with those obtained by other
researchers [58,64,65].
The desorption study of the adsorbents was carried out after the pro-
cess of Cr adsorption from the aqueous environment using sodium hy-
droxide (NaOH) solution with different concentrations (0.05–0.5 M)
for 2 h. The results are provided in Fig. S5. As the concentration of so-
dium hydroxide solution increased, the number of chromium ions sep-
arated from the adsorbent active sites increased. Maximum desorption
efficiencies for natural clay (98.14%), CS/Clay (98.23%), Clay/Fe3O4
The surfaces generated by the ANFIS for 4 types of adsorbents are
demonstrated in Figs. S6–9. Two indices of error rates and speed consid-
ered were used for the validation of the quality of prediction. The num-
ber of epochs for all runs was selected as 30 epochs. This number of
epochs guaranteed the accuracy of the results while preventing the
overflow of the optimization. Table 2 displays the error indices of opti-
mization. As can be seen, the R2 values for all trials (runs) are very
close to 1. The more the R2 value close to 1, the more valid outputs.
On the other hand, the values of MSE, SSE, and ARE, are b1. The smaller
the MSE, SSE, and ARE values, the more accurate the test results. Also,
Fig. 7 represents the comparison of the outputs of the ANFIS model
and laboratory results for the clay adsorbent. As can be seen, the results
of both are very close to each other. This indicates the good agreement
between the results predicted by ANFIS and the laboratory ones. By ex-
amining Fig. 7 and Table 2, it can be concluded that ANFIS has the capa-
bility to predict the removal efficiency of Cr pollutant by the clay based-
adsorbents, even if there are little laboratory results.
4. Conclusions
In the present work, magnetic nanoparticles of Fe3O4 and chitosan
were used to improve the adsorptive properties of natural clay in the
chromium (VI) removal from aqueous solution. The morphological,
magnetic, and physicochemical characteristics of the clay-based adsor-
bents (natural clay, CS/Clay, Clay/Fe3O4, and CS/Clay/Fe3O4) were thor-
oughly studied. The optimum value of contact time (30–60 min
depending on the adsorbent type), pH (2 or 3 depending on the adsor-
bent type) and adsorbent dose (2 g/L) for Cr(VI) adsorption were deter-
mined. Parameters determined from isotherm models like n, RL, and E
proposed that the Cr adsorption process is physically desirable. Both

Table 2
Error rates of the ANFIS prediction model.

Error rate Clay CS/Clay Clay/Fe3O4 CS/Clay/Fe3O4

Train Check Train Check Train Check Train Check

2
R 9.96E-01 7.15E-01 9.997E-01 9.32E-01 9.995E-01 6.435E-01 9.997E-01 8.21E-01
R 9.98E-01 8.46E-01 9.998E-01 9.66E-01 9.998E-01 8.022E-01 9.998E-01 9.06E-01
MSE 1.20E-05 1.22E-02 9.034E-07 1.66E-03 1.288E-06 9.862E-03 1.113E-06 3.55E-03
SSE 3.47E-03 1.11E-01 9.505E-04 4.o7E-02 1.135E-03 9.931E-02 1.055E-03 5.95E-02
ARE 5.30E-01 1.04E+01 8.943E-01 2.56E+00 5.594E+00 6.972E+00 1.215E+00 6.34E+00
364 R. Foroutan et al. / International Journal of Biological Macromolecules 151 (2020) 355–365
Fig. 7. The scatter plot of ANFIS model predicted values versus actual values for Cr(VI) adsorption onto clay.
parameters of Gibbs enthalpy and free energy were calculated to be
negative, indicating the exothermic and spontaneous of the adsorption
process, respectively. Sodium hydroxide solution with different concen-
trations was used to recover the adsorbents and the maximum desorp-
tion (~98%) was obtained at 0.5 M concentration. The reusability of clay-
based adsorbents was investigated up to 9Th steps. Also, the adsorbents
produced were used to clean the actual wastewater from the industrial
plant. Therefore, it can be suggested that natural clay, CS/Clay, Clay/
Fe3O4, and CS/Clay/Fe3O4 can be applied as suitable adsorbents for at-
tenuating chromium from aqueous solutions. Also, the results of this
survey revealed that the ANFIS model can be effectively used to predict
the efficiency of different adsorbents when there are few experimental
results for the training of the model prediction network.
CRediT authorship contribution statement
Rauf Foroutan: Formal analysis, Writing - original draft. Seyed
Jamaleddin Peighambardoust: Methodology, Validation. Reza
Mohammadi: Conceptualization, Methodology, Funding acquisition.
Mohsen Omidvar: Software, Validation. George A. Sorial: Supervision,
Writing - review & editing. Bahman Ramavandi: Supervision, Writing
- review & editing.
Declaration of competing interest
None.
Acknowledgments
This investigation was financially supported by the University of Ta-
briz (Grant No.: Tab-98-101) and technically supported by the Bushehr
University of Medical Sciences.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.ijbiomac.2020.02.202.
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