International Journal of Biological Macromolecules 182 (2021) 1138–1149

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International Journal of Biological Macromolecules

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

Preparation of EDTA-modified magnetic attapulgite chitosan gel bead

adsorbent for the removal of Cu(II), Pb(II), and Ni(II)
Ping Sun a, Wei Zhang a, Binze Zou a, Lincheng Zhou a,⁎, Zhengfang Ye b, Quanlin Zhao b
a
State Key Laboratory of Applied Organic Chemistry, College of Chemistry and Chemical Engineering, Lanzhou University, Lanzhou 730000, China
b
Department of Environmental Engineering, Peking University, The Key Laboratory of Water and Sediment Sciences, Ministry of Education, Beijing 100871, China

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

Article history: Attapulgite (ATP) has a unique porous layered chain structure and is an excellent environment-friendly decolor-
Received 25 February 2021 izer. However, its high viscosity makes it difficult to separate. First, it was combined with magnetic Fe3O4 nano-
Received in revised form 12 April 2021 particles to obtain Fe3O4-ATP that is easy to recycle and reuse. Then, Fe3O4-ATP nanoparticles were embedded in
Accepted 21 April 2021
chitosan (CS) gel beads, and glutaraldehyde was used for cross-linking and curing. Lastly, ethylenediaminetetra-
Available online 23 April 2021
acetic acid (EDTA) was successfully connected to Fe3O4-ATP/CS gel beads through amidation reaction, which fur-
Keywords:
ther increased the capability of the adsorbent to adsorb heavy metal ions. The prepared magnetic composite
Magnetic attapulgite adsorbent is a sphere with a rough surface and porous structure. The maximum adsorption capacity of the pre-
Chitosan bead pared Fe3O4-ATP/EDTA/CS adsorbent for Pb(II), Cu(II), and Ni(II) is 368.32, 267.94, and 220.31 mg g−1, respec-
EDTA modification tively. After 5 times of repeated use, Fe3O4-ATP/EDTA/CS still showed good adsorption capacity for Cu(II), Pb
(II), and Ni(II). Fe3O4-ATP/EDTA/CS has a large adsorption capacity for heavy metal ions, a wide pH applicability,
good reuse, and rapid magnetic separation. In addition, Cu(II) loaded Fe3O4-ATP/EDTA/CS also showed good cat-
alytic degradation performance for bisphenol A. This study prepared a new type of adsorbent with good adsorp-
tion performance and provided a promising method for the treatment of wastewater.
© 2021 Published by Elsevier B.V.

1. Introduction combination of organic materials can effectively promote the uniform

In modern society, environmental problems are becoming increas-
ingly serious, and the pollution of the water environment has become
the focus of attention of people. In consideration of the toxic and non-
biodegradable aspects of heavy metal ions in water [1], determining
how to treat heavy metal ions in sewage efficiently and economically
has been a research hotspot. The main technologies used to remove
heavy metal ions in wastewater are chemical precipitation [2], ion ex-
change [3], membrane filtration [4], electrochemical treatment [5], re-
verse osmosis [6], solvent extraction [7], and biological removal [8].
However, these methods are uneconomical. Adsorption is presently
considered the most attractive treatment technology due to its high ef-
ficiency, low cost, easy removal, and lack of secondary pollution [9,10].
Attapulgite (ATP) is a mineral rich in nature with a unique porous
layered chain structure. It is an excellent environment-friendly
decolorant, which can trap or adsorb colored substances and impurities
and form a large specific surface area inside and outside [11]. Therefore,
it has been widely used in wastewater treatment, sensors, coatings, and
catalyst carriers [12]. It has a net negative charge and can remove cat-
ions from wastewater to meet discharge standards [13]. The
⁎ Corresponding author.
E-mail address: zhoulc@lzu.edu.cn (L. Zhou).
dispersion of ATP and its surface adhesion and adsorption [14]. Organic
hybrid forms mainly include complexes of surfactants, silane coupling
agents, and organic polymer materials [15]. But it has the shortcomings
of high viscosity and difficult separation, so this shortcoming needs to
be solved in practical applications. Magnetic Fe3O4 nanoparticles can
be easily dispersed in water or other organic systems by simple stirring
or shaking [16]. These particles can be sufficiently separated and re-
moved from liquid via an external magnetic field without using compli-
cated operations [17]. In this study, in order to improve the
shortcomings of ATP, ATP was modified by chemical co-precipitation
using Fe3O4. As a typical example, Lu et al. synthesized a magnetic
attapulgite adsorbent and its maximum adsorption capacity for Eu(III)
could reach 4.94 × 10−4 mol g−1 [18]. From the perspective of adsorp-
tion capacity, this bare magnetic attapulgite nanocomposite has a low
adsorption capacity and is not a good choice for practical applications.
Therefore, it is of great significance to modify the original magnetic
attapulgite nanocomposite to adjust its adsorption capacity or improve
efficiency to meet the requirements of practical applications.
Chitosan (CS), as a deacetylated product of chitin, has attracted
much attention because of its cost-effectiveness, wide sources,
nontoxicity, biocompatibility, and biodegradability [19]. For example,
its abundant functional groups (such as −NH2 and −OH) with strong
complexing capability on its molecular backbone make it become a

https://doi.org/10.1016/j.ijbiomac.2021.04.132
0141-8130/© 2021 Published by Elsevier B.V.
P. Sun, W. Zhang, B. Zou et al.
promising adsorbent for cationic heavy metal absorption [20–25]. At the
same time, CS is easily formed into different block structures and can be
used as a carrier for ATP immobilization to make the material have a cer-
tain hardness and shape. In actual production, a peristaltic pump can be
used to transport polysyrup, and then solidify in the coagulation solu-
tion (NaOH). It can be more convenient in practical applications. Ethyl-
enediaminetetraacetic acid (EDTA) is known for its effective removal of
heavy metals through metal complexation mechanisms [26]. However,
after complexing with heavy metal ions, its mobility will increase, caus-
ing metal ions to leak into the environment and affecting ecological
safety and human health [27]. Thus, EDTA must be immobilized to en-
sure operability by cross-linking onto the surface of an insoluble solid
support [28] or to form an insoluble substance [29] for practical use.
Fe3O4-ATP nanoparticles were prepared to improve the disadvan-
tages of high viscosity and difficult separation of ATP. The Fe3O4-ATP
nanoparticles were embedded in CS gel beads, and glutaraldehyde
was used for cross-linking and curing; hence, they have a large specific
surface area and certain hardness. The addition of the −NH2 group of CS
enhanced the adsorption performance of Fe3O4-ATP. EDTA was success-
fully linked to Fe3O4-ATP/CS gel beads through an amidation reaction,
which increased the adsorption performance of the adsorbent. The
maximum adsorption capacity of Fe3O4-ATP/EDTA/CS adsorbent for Cu
(II), Pb(II), and Ni(II) exceeds that reported in most works. At
the same time, its magnetic separation, good stability, and wide pH ap-
plicability further provide the possibility for its handling of heavy metal
ions in practical applications. In addition, Cu(II) loaded Fe3O4-ATP/
EDTA/CS also showed good catalytic degradation performance for
bisphenol A. This provides further possibilities for its use in wastewater
treatment.
2. Experimental sections
2.1. Materials and instruments
Attapulgite came from Kaidi Company (Gansu, China). Chitosan
(≥95% degree of deacetylation) was got from Aladdin. N-
hydroxysuccinimide (NHS) and 1-ethyl-3-(3-dimethylaminopropyl)
carbodiimide (EDC) were purchased from Shanghai Macklin Biochemi-
cal Technology Co., Ltd. Other organic reagents were obtained from
Sigma-Aldrich. All reagents in this work were analytically pure, and
the water used was deionized water. Ion concentration meters of Cu
(II) (HI96702) and Ni(II) (HI96740) were produced in Italy HANNA,
Pb(II) concentration meter (PB-2A) was created by Haiheng Electrome-
chanical Instrument Co., Ltd. (Shanghai, China).
2.2. Purification of ATP
ATP was weighed into 5 mol L−1 sulfuric acid solution and stirred at
80 °C for 1 h. After collecting it, it was washed with water to pH = 7, fil-
tered, and dried. Then, it was added to a sodium hexametaphosphate
solution (3 wt%) under magnetic stirring. The solution was sonicated
for 1 h, standing still, and the upper solution was decanted. After centrif-
ugal dehydration, drying, and grinding, the purified ATP was obtained.
2.3. Preparation of magnetic ATP
Magnetic ATP was synthesized using a coprecipitation method [30].
Purified ATP (1.5 g) was weighed into 50 mL of water, then 4.41 g of
FeCl3·6H2O and 1.61 g of FeCl2·4H2O were added. In a N2 atmosphere,
the mixed solution was stirred and heated to 80 °C, 6 mL of ammonia
(25 wt%) was added dropwise, and the reaction was performed for 1 h
to obtain a magnetic ATP powder. The powder was filtered, washed
with water, and dried under vacuum to obtain Fe3O4-ATP.
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International Journal of Biological Macromolecules 182 (2021) 1138–1149
2.4. Preparation of Fe3O4-ATP/CS
CS (0.3 g) was dissolved in 10.0 mL of an acetic acid solution (2 wt%),
then 0.3 g of magnetic ATP was sonicated for 20 min to disperse it in the
CS solution. Subsequently, it was added dropwise to 1 M NaOH solution
with a syringe, left to stand for 5 h, filtered, washed with water to neu-
trality, and soaked in 5% glutaraldehyde solution for 4 h. After cross-
linking and curing, it was filtered, washed, and freeze-dried to obtain
Fe3O4-ATP/CS gel beads.
2.5. EDTA functionalization
Fe3O4-ATP/CS was modified using EDTA through amidation reaction
[31]. Na2EDTA (2 g) was added to 40 mL of water to dissolve completely
via sonication, 0.1 g of EDC and 0.2 g of NHS were added, and stirring
was performed for 1 h. Fe3O4-ATP/CS microspheres (0.2 g) were dis-
persed into the above solution by mechanical stirring for 2 h. The ob-
tained black product was washed several times with water and
vacuum dried at 50 °C to obtain Fe3O4-ATP/EDTA/CS gel beads.
2.6. Solid state characterization
The morphology of the materials was characterized by SEM (JSM-
6701F). The specific surface area of the materials was measured at liquid
N2 temperature (76 K) using a Micromeritics ASAP 2010M apparatus.
FT-IR spectra were obtained from FT-IR spectrometer (Model 170-SX,
American Nicolet Corp.). The TGA curves of the materials were obtained
from comprehensive thermal analyzer (PT1600). Magnetic hysteresis
loops were obtained using vibrating sample magnetometry (VSM,
LAKESHORE-7304, USA). The X-ray photoelectron spectroscopy (XPS)
was carried out through an ESCALab220i-XL electron spectrometer
(VG Scientific) with 300 W Al-Kα radiation and X-ray diffraction
(XRD) spectra were obtained from Rigaku D/MAX-2400 with Ni-
filtered Cu-Kα radiation.
2.7. Adsorption experiment
2.7.1. Effect of pH
Fe3O4-ATP/CS and Fe3O4-ATP/EDTA/CS gel beads (25 mg) were
added to 50 mL 100 mg L−1 of Cu(II), Pb(II), and Ni(II) solutions. A
HCl solution (1 M) was used to adjust the pH of the solutions to 1–6.
The mixed solutions were shaken for 4 h at 250 rpm at room tempera-
ture. The concentration changes of Cu(II), Pb(II), and Ni(II) were mea-
sured using an ion concentration meter.
2.7.2. Effect of adsorbent concentration
Fe3O4-ATP/EDTA/CS gel beads (5, 10, 15, 25, 50, and 75 mg) were
added to 50 mL 100 mg L−1 of Cu(II), Pb(II), and Ni(II) solutions. The
pH of the solutions was adjusted to 5 with 1 M HCl solution. The
mixed solutions were shaken for 4 h at 250 rpm at room temperature.
The concentration changes of Cu(II), Pb(II), and Ni(II) were measured
using an ion concentration meter.
2.7.3. Effect of ionic strength
Fe3O4-ATP/EDTA/CS gel beads (15 mg) were added to 50 mL 100 mg
L−1 of Cu(II), Pb(II), and Ni(II) solutions, and the pH value of the solu-
tions was adjusted to 5 with 1 M HCl solution. NaCl powder of different
quality was added to the solutions to adjust the ionic strength. The
mixed solutions were shaken for 4 h at 250 rpm at room temperature.
The concentration changes of Cu(II), Pb(II), and Ni(II) were measured
using an ion concentration meter.
2.7.4. Adsorption kinetics
Fe3O4-ATP/EDTA/CS gel beads (25 mg) were added to 100 mL
100 mg L−1 of Cu(II), Pb(II), and Ni(II) solutions, and the pH value of
the solutions was adjusted to 5 with 1 M HCl solution. The mixed
P. Sun, W. Zhang, B. Zou et al.
solutions were shaken at 250 rpm at room temperature and removed at
intervals. The concentration changes of Cu(II), Pb(II), and Ni(II) were
measured using an ion concentration meter.
2.7.5. Adsorption isotherms and thermodynamics
Cu(II), Pb(II), and Ni(II) solutions were prepared with a concentra-
tion range of 0.1–1 g L−1. Fe3O4-ATP/EDTA/CS gel beads (15 mg) were
added to 50 mL of Cu(II), Pb(II), and Ni(II) solutions of different concen-
trations, and the pH value of the solutions was adjusted to 5 with 1 M
HCl solution. The mixed solutions were shaken for 4 h at 250 rpm at
15 °C, 25 °C, and 35 °C. The concentration changes of Cu(II), Pb(II),
and Ni(II) were measured using an ion concentration meter.
2.7.6. Repetitive experiment
HCl solution (0.1 mol L−1) was used as a desorbent, and Cu(II)-, Pb
(II)-, and Ni(II)-supported composites could be desorbed. Heavy
metal-loaded sorbent (50 mg) was added to 50 mL of HCl solution,
and the mixture was placed in a thermostatic shaker. At the end of the
operation, it was filtered, and the solid was washed several times with
water and used for another adsorption.
2.7.7. Competitive adsorption
Fe3O4-ATP/EDTA/CS gel beads (25 mg) were added to 25 mL 100 mg
L−1 of Cu(II), Pb(II), Ni(II), Cu(II)–Pb(II), Cu(II)–Ni(II), Pb(II)–Ni(II), and
Cu(II)–Pb(II)–Ni(II) solutions, and the pH value of the solutions was ad-
justed to 5 with 1 M HCl solution. The mixed solutions were shaken for
4 h at 250 rpm at room temperature. The concentration changes of Cu
(II), Pb(II), and Ni(II) were measured with an ion concentration meter.
The following two formulas express the adsorption capacity of the
adsorbent.
ðC 0 −C t ÞV
qt ¼
m
ðC 0 −C t Þ
Removal efficiencyð%Þ ¼
C0
where C0 (mg L−1) and Ct (mg L−1) are the concentration of the adsor-
bate at the initial and t, respectively, V (L) represents the volume of the
solution, and m (g) is the mass of the adsorbent.
Fig. 1. Schematic representation of the preparation of Fe3O4-ATP/EDTA/CS gel beads.
International Journal of Biological Macromolecules 182 (2021) 1138–1149
3. Results and discussion
3.1. Preparation and characterization of composites
As shown in Fig. 1, the preparation of Fe3O4-ATP/EDTA/CS gel beads
are mainly divided into three steps. First, Fe3O4-ATP was prepared by
coprecipitation reaction. Then, the mixed solution of magnetic ATP
and CS was added dropwise to a NaOH solution. The formation of
Fe3O4-ATP/CS hydrogel beads is based on the combination of the breath
figure phenomenon with the coprecipitation reaction [32]. When hy-
droxide ions diffuse in a mixture of magnetic ATP and CS and are neu-
tralized with acetic acid, the interaction of magnetic ATP and CS
provides sufficient interfacial tension, which makes the hexagonal
water droplets an ordered matrix at the interface. When the water
droplets leave the interface, a multilayer honeycomb structure is
formed [32]. The magnetic ATP powder was fixed in CS, and the use of
glutaraldehyde as a cross-linking agent increased the hardness of
Fe3O4-ATP/CS [26]. Lastly, through the amidation reaction between
the amino group of CS and the carboxyl group of EDTA, EDTA was
grafted onto the Fe3O4-ATP/CS composite material to form Fe3O4-ATP/
EDTA/CS gel beads [31]. The adsorbent prepared in the work is a mag-
netic ball, which is convenient for recycling. The organically modified
Fe3O4-ATP/EDTA/CS gel beads have multiple functional groups that
can bind heavy metals.
3.2. Characterization
A scanning electron microscope was used to determine the mor-
phology of ATP, Fe3O4-ATP, Fe3O4-ATP/CS, and Fe3O4-ATP/EDTA/CS
materials. As shown in Fig. 2a, ATP has a rod-like structure after acid pu-
ð1Þ rification. Fig. 2b depicts that Fe3O4 magnetic nanoparticles are coated
on the surface of ATP, and the rod-like structure of ATP becomes consid-
erably disordered. CS will immediately form a gel in an alkaline solu-
ð2Þ tion; hence, the preparation by using a dropper can well control the
material shape to be spherical (Fig. 2c, e). After the magnetic ATP is
mixed into the CS beads, the material surface (Fig. 2d) shows a honey-
comb structure. Fig. 2e and f illustrate that after the Fe3O4-ATP/CS gel
beads are modified with EDTA, the size of the gel ball is slightly in-
creased, and the pores on the material surface decrease. This condition
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P. Sun, W. Zhang, B. Zou et al.
Fig. 2. SEM images of ATP (a), Fe3O4-ATP (b), Fe3O4-ATP/CS (c, d) and Fe3O4-ATP/EDTA/CS (e, f) gel beads.
indicates that EDTA is successfully grafted with the CS evenly distrib-
uted inside and outside the gel beads.
Fig. 3 shows the N2 adsorption–desorption isotherms and BJH pore
size distributions of Fe3O4-ATP/CS and Fe3O4-ATP/EDTA/CS gel beads.
The specific surface areas of Fe3O4-ATP/CS and Fe3O4-ATP/EDTA/CS cal-
culated using the BET method are 130.65 and 51.81 m2 g−1, respec-
tively; the pore volumes calculated using the BJH method are 0.496
and 0.225 cm3 g−1, respectively. EDTA molecules are cross-linked
with the amino group of CS, which leads to reductions in surface area
and pore volume; this result is consistent with the results reported by
Repo et al. [34].
FT-IR was performed on ATP, Fe3O4-ATP, Fe3O4-ATP/CS, and Fe3O4-
ATP/EDTA/CS materials to confirm the structural information of the ob-
tained magnetic materials. In Fig. 4a, 984.8 and 1030.6 cm−1 correspond
to the Si\\O of ATP symmetric tensile vibration and stretching vibration
bands, respectively [35]. The vibration band of 1655.6 cm−1 belongs to
that of ATP-adsorbed water and zeolite water. The bands at 3614.6
and 3551.6 cm−1 are the hydroxyl stretching vibration and out-of-
plane bending vibration of structural water, respectively; 3417.9 cm−1
is the stretching vibration band of the hydroxyl functional group that
connects the Mg and Al between the tetrahedral and octahedral struc-
tures in the structural water [36]. 571.3 and 508.4 cm−1 are the
Fig. 3. The N2 adsorption-desorption isotherms (a) and BJH pore size distribution (b) of Fe3O4-ATP/CS and Fe3O4-ATP/EDTA/CS.
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International Journal of Biological Macromolecules 182 (2021) 1138–1149
vibration bands of the Fe\\O functional group in Fe3O4 structure [37].
the vibration band of 3421.2 cm−1 is caused by the tensile vibration of
the N\\H and O\\H functional groups, and the vibration bands at
2937.8 and 2873.1 cm−1 come from the tensile vibration of the C\\H
bond. The bands at approximately 1718.1, 1591, and 1362.9 cm−1 can
be interpreted as amide I, amide II, and CH3 symmetrical angular defor-
mation, respectively [38]. For Fe3O4-ATP/CS, the characteristic vibration
bands of Fe3O4-ATP and CS appear at the same time; some vibration
bands of CS weaken; a strong C=N vibration band appears at 1663.0
cm−1, which is attributed to the cross-linking reaction between CS
and glutaraldehyde [39]. For Fe3O4-ATP/EDTA/CS, the 1631.4 cm−1
band is attributed to the tensile vibration of the carbonyl group in
−COO−. The characteristic band near 1398.1 cm−1 from the C\\O func-
tional group in −COO−[40] indicates that the carboxyl group in EDTA is
successfully introduced into Fe3O4-ATP/CS.
The TGA curves of the sample are shown in Fig. 4b. The final mass
losses of ATP, Fe3O4-ATP, Fe3O4-ATP/CS, and Fe3O4-ATP/EDTA/CS are
16.62%, 15.96%, 61.6%, and 71.2%, respectively. The weight loss for ATP
and Fe3O4-ATP comes entirely from physically adsorbed water or/and
structured water evaporation with increasing temperature. For Fe3O4-
ATP/CS and Fe3O4-ATP/EDTA/CS, in addition to water loss at lower tem-
perature, organic polymers begin to decompose rapidly above 250 °C;
P. Sun, W. Zhang, B. Zou et al.
Fig. 4. FT-IR spectra (a), TGA curves (b), XRD patterns (c) and VSM curves (d) of ATP, Fe3O4-ATP, Fe3O4-ATP/CS and Fe3O4-ATP/EDTA/CS.
this result is consistent with the result obtained by M. Monier et al. [38].
In the temperature range of 250 °C–800 °C, the weight loss of Fe3O4-
ATP/CS is 21.1%, and the weight loss of Fe3O4-ATP/EDTA/CS is 22.9%.
This condition reflects the content of CS in the prepared material. In
this temperature range, the weight loss of Fe3O4-ATP/EDTA/CS is higher
than that of Fe3O4-ATP/CS, which proves that EDTA is successfully con-
nected to the CS surface.
Fig. 4c shows the XRD patterns of ATP, Fe3O4-ATP, Fe3O4-ATP/CS, and
Fe3O4-ATP/EDTA/CS to clarify the crystalline properties of the materials.
In Fig. 4c, the sharp diffraction peaks of ATP at 2θ = 19.6°, 27.48° belong
to the (040) and (400) planes, respectively [41]. The five distinct diffrac-
tion peaks observed at 2θ = 30.29°, 35.53°, 42.92°, 57.04° and 62.87°
correspond to (220), (311), (400), (511) and (440), respectively,
which conform to the spinel structure of Fe3O4 (JCPDS card 19-629)
[42]. This result shows that the addition of ATP does not change the
structure of Fe3O4 nanoparticles. For Fe3O4-ATP/EDTA/CS and Fe3O4-
ATP/CS, the two curves have the same characteristic peaks at 19.8°
and 35.53° representing the CS and Fe3O4 spinel structures [43,44], re-
spectively. Therefore, XRD analysis shows that the modification of
EDTA does not change the natural crystal structure of Fe3O4-ATP/CS.
XPS was used to identify the properties of elements in Fe3O4-ATP/
EDTA/CS gel beads. The signal peak appearing at 100.65 eV in Fig. 5a be-
longs to Si 2p3/2 in ATP. In Fig. 5b, the signal of Fe 2p is composed of two
peaks, and their binding energies are 722.31 and 708.85 eV, which rep-
resent Fe 2p1/2 and Fe 2p3/2, respectively; the peak of Fe 2p3/2 can be di-
vided into two peaks with binding energies of 708.66 eV (belonging to
Fe2+) and 713.04 eV (belonging to Fe3+) [45]. Fig. 5c presents the
high-resolution XPS spectra of N 1 s. The N peaks at 396.95, 398.01,
and 399.62 eV represent N\\C, −NH/−NH2, and −NH+ 3 [24,46], respec-
tively. In Fig. 5d, the characteristic peak of O 1s is composed of three ab-
sorption peaks with binding energies of 528.59 eV (belonging to O=C–
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International Journal of Biological Macromolecules 182 (2021) 1138–1149
O−), 529.80 eV (belonging to C–O–C), and 530.69 eV (belonging to C–
O–H) [47–49]. The absorption peak at 528.59 eV proves that EDTA is at-
tached to the surface of Fe3O4-ATP/CS gel sphere through amidation
reaction.
The magnetic hysteresis loops of the fabricated materials are shown
in Fig. 4d. Fe3O4-ATP, Fe3O4-ATP/CS, and Fe3O4-ATP/EDTA/CS all exhibit
superparamagnetism, which indicates that the coated organic sub-
stance inconsiderably changes the magnetic properties. The saturation
magnetization (Ms) values of Fe3O4-ATP, Fe3O4-ATP/CS, and Fe3O4-
ATP/EDTA/CS are 25.5, 3.2, and 0.9 emu g−1, respectively. The decrease
in the saturation magnetization of the sample is due to the introduction
of nonmagnetic CS and EDTA, which proves that the organic layer is suc-
cessfully coated on the surface of the magnetic ATP. Although the satu-
ration magnetization of the sample is small, it can still perform magnetic
separation within a few minutes in the presence of an additional mag-
netic field to achieve the purpose of recycling.
3.3. Effect of pH
Cu(II), Pb(II), and Ni(II) can form hydroxide precipitates under alka-
line conditions; thus, Fe3O4-ATP/CS and Fe3O4-ATP/EDTA/CS gel beads
were added to Cu(II), Pb(II), and Ni(II) solutions; the initial pH value
of the solutions was adjusted with hydrochloric acid to 1, 2, 3, 4, 5,
and 6 [50], and the adsorption result is shown in Fig. 6a. As shown in
Fig. 6a, when pH < 4, the adsorption capacity increases with increasing
pH; when pH > 4, the adsorption capacity of the adsorbent tends to be
stable. Fe3O4-ATP/EDTA/CS gel beads have a higher adsorption capacity
for these metal ions in a wider pH range. EDTA has a strong chelating ca-
pability for a wide range of Cu(II), Pb(II), and Ni(II) ions. Therefore, the
modification of EDTA on the surface of Fe3O4-ATP/CS gel beads can
greatly improve the adsorption capacity. Fig. 6a shows that the optimal
P. Sun, W. Zhang, B. Zou et al. International Journal of Biological Macromolecules 182 (2021) 1138–1149

Fig. 5. XPS spectra of Fe3O4-ATP/EDTA/CS, full spectrum (a), Fe 2p (b), N 1s (c) and O 1s (d).

pH for Fe3O4-ATP/EDTA/CS and Fe3O4-ATP/CS gel beads is 5. Fe3O4-ATP/
CS and Fe3O4-ATP/EDTA/CS contain substantial amino groups, which
are protonated in aqueous solution to make the system positively
charged. At low pH, the positive charge increases, the electrostatic re-
pulsion with metal cations increases, and the adsorption performance
decreases (Fig. 6b). The enhancement in adsorption performance at
high pH may be due to the decrease in the number of positively charged
groups in the solutions. Compared with Fe3O4-ATP/CS, Fe3O4-ATP/
EDTA/CS introduces negatively charged carboxyl groups, the positive
charge decreases, and the adsorption performance increases.
3.4. Effect of sorbent concentration
Fe3O4-ATP/EDTA/CS gel beads with different masses were added to
Cu(II), Pb(II), and Ni(II) solutions. The adsorption effect is described in
Fig. 7. Fig. 7a and b indicate that with the increase in the amount of
Fe3O4-ATP/EDTA/CS gel beads added, the removal rate of heavy metal
ions is considerably enhanced, but the adsorption capacity decreases.
As the amount of sorbent increases, the number of active sites provided
increases, and the removal rate enhances. Nevertheless, the increase in
the dosage to a certain concentration does not contribute much to the

Fig. 6. The effect of pH on the adsorption of heavy metal ions by Fe3O4-ATP/CS and Fe3O4-ATP/EDTA/CS (a) and the zeta potential of Fe3O4-ATP/CS and Fe3O4-ATP/EDTA/CS (b).

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P. Sun, W. Zhang, B. Zou et al.
Fig. 7. The effect of Fe3O4-ATP/EDTA/CS concentration on its adsorption of heavy metal ions.
removal rate due to the limited number of pollutants. In consideration
of the effects of adsorbent concentration and the removal rate of
heavy metal ions, the concentration of Fe3O4-ATP/EDTA/CS is set to
0.3 g L−1 in the experiment to determine the maximum adsorption
capacity.
3.5. Effect of ionic strength
The ionic strength in the solution will affect the adsorption of heavy
metal ions. Fig. 8 depicts that the adsorption capacity of Fe3O4-ATP/
EDTA/CS for Cu(II), Pb(II), and Ni(II) gradually decreases as the ionic
strength increases when the concentration of NaCl is 0–3.0 mol L−1.
Ion exchange competition occurs between the electrolyte ion Na
(I) and the adsorbed metal cation; consequently, the increase in ionic
strength suppresses the adsorption.
3.6. Effects of contact time and adsorption kinetics
The effect of contact time on the adsorption of Cu(II), Pb(II), and Ni
(II) by Fe3O4-ATP/EDTA/CS is shown in Fig. 9a. The adsorption process
is considerably fast at first, then gradually slows down after 15 min,
and finally reaches equilibrium after 60 min. Pseudo-first- and
-second-order models are used to process the kinetic data and study
Fig. 8. The effect of ionic strength on adsorption of Fe3O4-ATP/EDTA/CS for heavy metals.
1144
International Journal of Biological Macromolecules 182 (2021) 1138–1149
the rate control step in the adsorption mechanism. Eqs. (3) and (4)
are the equations of the two dynamic models [51,52].
ln ðqe −qt Þ ¼ ln qe −k1 t ð3Þ
t 1 t
¼ þ ð4Þ
qt k2 q2e qe
where qt (mg g−1) and qe (mg g−1) are the adsorption capacities at t and
equilibrium, respectively. t (min) is the adsorption time, k1 (min−1) is
the pseudo-first-order rate constant, and k2 (g mg−1 min−1) is the
pseudo-second-order rate constant.
The reaction kinetics of Fe3O4-ATP/EDTA/CS is shown in Fig. 9b, and
the kinetic parameters are shown in Table 1. The table indicates that the
pseudo-second-order kinetic equation can clearly describe the process
of Fe3O4-ATP/EDTA/CS adsorption of Cu(II), Pb(II), and Ni(II). The rea-
son is that the correlation coefficient (R2) of the pseudo-second-order
kinetic model is closer to 1 than that of the pseudo-first-order kinetic
model. qe,cal value calculated from the pseudo-second-order equation
is also closer to the experimental value qe,exp, which indicates that
chemical adsorption is the main rate-controlling step in the adsorption
mechanism of Fe3O4-ATP/EDTA/CS [52].
In addition, the Elovich equation can be used to describe the adsorp-
tion behavior of highly homogeneous adsorbents.
1 1
Qt ¼ ln ðαβÞ þ ln t ð5Þ
β β
where α (mg g−1 min−1) represents the initial adsorption rate, and β (g
mg−1) represents the desorption constant. Table S1 shows the parame-
ter values of the Elovich model. Compared with the pseudo-first-order
and pseudo-second-order models, the Elovich model does not describe
the adsorption behavior very well.
3.7. Adsorption isotherm
The adsorption isotherm can reflect the interaction mode between
adsorbent and adsorbate, further explaining the adsorption mechanism.
The isotherms of Fe3O4-ATP/EDTA/CS and Fe3O4-ATP/CS adsorbing Pb
(II), Cu(II), and Ni(II) at 298 K are shown in Fig. 10(a–c). These figures
suggest that the maximum adsorption capacities of Fe3O4-ATP/EDTA/
CS for Pb(II), Cu(II), and Ni(II) are 368.32, 267.94, and 220.31 mg g−1,
respectively; the maximum adsorption capacities of Fe3O4-ATP/CS for
Pb(II), Cu(II), and Ni(II) are 224.15, 144.47, and 105.56 mg g−1, respec-
tively. This result indicates that the chelation of EDTA further increases
the adsorption capacity of the adsorbent.
Langmuir and Freundlich adsorption isotherms can describe the ad-
sorption process of substances. Their equations are shown as follows:
P. Sun, W. Zhang, B. Zou et al. International Journal of Biological Macromolecules 182 (2021) 1138–1149

Fig. 9. The effect of contact time on the adsorption of heavy metal ions by Fe3O4-ATP/EDTA/CS (a) and pseudo-second order kinetic cruves (b).

1
Table 1 log qe ¼ log K F þ log C e ð7Þ
Kinetic model parameters of adsorption of heavy metal ions by Fe3O4-ATP/EDTA/CS at 25 n
°C.
where qe (mg g−1) is the adsorption capacity at equilibrium, Ce (mg
Adsorbate C0 qe,exp Pseudo-first order Pseudo-second order
L−1) is the concentration at equilibrium, KL (L mg−1) is the adsorption
(mg (mg kinetics kinetics
L−1) g−1) equilibrium constant of the Langmuir isothermal model, and qm (mg
R2 R2
qe,cal k1 qe,cal k2
g−1) is the maximum adsorption capacity. KF and n are the empirical
(mg (min−1) (mg (g mg−1 constants of the Freundlich isothermal model, indicating the relative ad-
g−1) g−1) min−1) sorption capacity and adsorption intensity, respectively. The relevant
Pb(II) 100 155.62 69.01 0.073 0.9518 160.00 0.0028 0.9998 parameters are shown in Table 2. The Langmuir model can better fit
Cu(II) 100 142.60 76.46 0.109 0.9894 145.59 0.0025 0.9978 the experimental data compared with the Freundlich model because
Ni(II) 100 129.58 65.91 0.091 0.7958 138.89 0.0012 0.9967
the Langmuir model has a higher correlation coefficient (R2) and maxi-
mum adsorption amount (qm) closer to the experimental value. This re-
sult indicates that the Fe3O4-ATP/EDTA/CS and Fe3O4-ATP/CS
Ce 1 Ce adsorption of Cu(II), Pb(II), and Ni(II) is a monolayer adsorption, and
¼ þ ð6Þ
qe qm K L qm the adsorbent surface is uniform with the same adsorption site [53].

Fig. 10. Adsorption isotherms of Fe3O4-ATP/EDTA/CS and Fe3O4-ATP/CS for Pb(II) (a), Cu(II) (b) and Ni(II) (c) at 298 K; the fitting curves of Langmuir model of the adsorption of Fe3O4-ATP/
EDTA/CS and Fe3O4-ATP/CS for Pb(II) (d), Cu(II) (e) and Ni(II) (f).

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Table 2
Langmuir and Freundlich adsorption model parameters of Fe3O4-ATP/CS and Fe3O4-ATP/EDTA/CS adsorbing heavy metal ions at 25 °C.

Adsorbent Adsorbate Langmuir model Freundlich model

qm kL R2 RL kF n R2

(mg g−1) (L mg−1) ((mg g−1) (L mg−1))1/n

Fe3O4-ATP/CS Pb(II) 227.79 0.343 0.9999 0.0029–0.0045 131.95 8.87 0.8523

Cu(II) 166.67 0.0266 0.9956 0.0544–0.4577 9.88 1.88 0.9198
Ni(II) 133.33 0.0164 0.9873 0.1037–0.5840 5.76 1.79 0.9758
Fe3O4-ATP/EDTA/CS Pb(II) 371.75 0.7173 0.9995 0.0013–0.0019 272.52 15.43 0.8500
Cu(II) 285.71 0.0593 0.9950 0.0175–0.1188 39.03 2.55 0.9013
Ni(II) 232.56 0.0746 0.9958 0.0162–0.1130 34.03 2.55 0.7992

Fig. 11. The fitting curves of Langmuir model of the adsorption of Fe3O4-ATP/EDTA/CS for Pb(II) (a), Cu(II) (b) and Ni(II) (c) at 288 K, 298 K and 308 K, respectively.

Table S2 compares the adsorption performance of the adsorbent in this

work with that of other adsorbents reported. ΔG0 ¼ −RT ln K d ð10Þ
The separation factor constant (RL) is used to evaluate the suitability
of the sorbent studied. RL is defined as follows: ΔS0 ΔH 0
ln K d ¼ − ð11Þ
R RT
1
RL ¼ ð8Þ where R (8.314 J mol−1 K−1) and T (K) are the gas constant and absolute
1 þ KLC0
temperature, respectively. The equilibrium constant Kd can be obtained
where KL (L mg−1) is the adsorption equilibrium constant of the Lang- as following:
muir isothermal model, and C0 (mg g−1) is the initial concentration. qe
Therefore, the magnitude of RL value represents the feasibility of ad- Kd ¼ ð12Þ
Ce
sorption. As shown in Table 2, 0 < RL < 1 indicates that Fe3O4-ATP/
EDTA/CS and Fe3O4-ATP/CS are beneficial to the adsorption of Cu(II), where Ce (mg L−1) and qe (mg g−1) are the equilibrium concentration of
Pb(II), and Ni(II) [54]. the adsorbed substance in the solution and the equilibrium adsorption
The Temkin equation assumes that the binding energy has a uniform capacity of the adsorbed substance, respectively. ΔS0 and ΔH0 can be ob-
distribution, so the maximum binding energy can be reached during the tained from the intercept and slope of the plot of lnKd versus 1/T,
adsorption process. The Temkin isotherm is usually given by the Eq. (9): respectively.
Table 3 lists the values of the thermodynamic parameters. ΔG0
Q e ¼ Bt ln K t þ Bt ln C e ð9Þ values at different temperatures are negative, indicating that the ad-
sorption process is spontaneous. ΔG0 value decreases with increasing
where Kt (L mg−1) represents the equilibrium binding constant, which
corresponds to the maximum binding energy. Table S3 shows the pa- Table 3
rameter values of the Temkin model. Compared with Langmuir and Thermodynamic parameters of heavy metal ions adsorption by Fe3O4-ATP/EDTA/CS.
Freundlich's R2, the Langmuir model describes the adsorption process
Adsorbate Temperature ΔG0 ΔH0 ΔS0
better.
−1 −1
(K) (kJ mol ) (kJ mol ) (J mol−1 K−1)

3.8. Adsorption thermodynamics Pb(II) 288 −14.40 8.21 46.03

298 −14.86
308 −15.32
The adsorption isotherms were measured at 288 K, 298 K, and 308 K
Cu(II) 288 −10.89 9.89 34.83
to evaluate the thermodynamic characteristics of the target adsorbate 298 −11.24
on the Fe3O4-ATP/EDTA/CS adsorbent. As shown in Fig. 11, the adsorp- 308 −11.59
tion capacity increases as the temperature increases. The analysis of Ni(II) 288 −3.47 5.04 11.09
the adsorption isotherm data by using Eqs. (10) and (11) can indicate 298 −3.58
308 −3.69
the thermodynamic parameters (ΔG0, ΔH0, and ΔS0).

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P. Sun, W. Zhang, B. Zou et al. International Journal of Biological Macromolecules 182 (2021) 1138–1149

Fig. 12. Reusability of Fe3O4-ATP/EDTA/CS for Cu(II), Pb(II) and Ni(II) (a), and percentage removal of Cu(II), Pb(II) and Ni(II) from single, binary and ternary mixtures (b).

temperature, which means that high temperature is beneficial to the ad- 3.9. Reuse performance
sorption process. Positive ΔH0 indicates that the adsorption process is
endothermic. Positive ΔS0 means that the randomness at the interface From Fig. 12a, the adsorption capacity of Fe3O4-ATP/EDTA/CS gel
of the solid or liquid increases during the adsorption process [55]. beads for Cu(II), Pb(II), and Ni(II) decreases slightly after repeated use

Fig. 13. XPS (a), N 1s (b), O 1s (c) spectra of Fe3O4-ATP/EDTA/CS before and after Cu(II), Pb(II) and Ni(II) adsorption, and Schematic diagram of the process of removing when Fe3O4-ATP/
EDTA/CS was used as adsorbent and catalyst (d).

1147
P. Sun, W. Zhang, B. Zou et al.
Table 4
Removal rate of Fe3O4-ATP/EDTA/CS under different conditions to BPA.
Fe3O4-ATP/EDTA/CS
Removal rate (%) 4 11
Reaction conditions: Initial concentration of BPA: 70 mg L−1, volume of solution: 20 mL, material dosage: 10 mg, H2O2 dosage: 1 mL (30%), initial solution pH: 7.0, temperature: 298 K,
speed: 250 rpm, and time: 2 h.
for 5 times. After 5 cycles, Fe3O4-ATP/EDTA/CS can still adsorb 92%, 90%,
and 89% of Pb(II), Cu(II), and Ni(II), respectively. Thus, Fe3O4-ATP/
EDTA/CS gel beads have high stability and a good application prospect
in the adsorption of heavy metal ions.
3.10. Multicomponent adsorption
The removal rates of heavy metal ions in single, binary, and ternary
systems are shown in Fig. 12b to compare the adsorption capacity of
the prepared adsorbent for Cu(II), Pb(II), and Ni(II). In the unitary sys-
tem, the removal rates of Fe3O4-ATP/EDTA/CS for Pb(II), Cu(II), and Ni
(II) are 98%, 84%, and 71%, respectively. In the mixed solutions of Pb
(II)–Cu(II) and Pb(II)–Ni(II), the removal rates of Pb(II) decrease to
94% and 96%, respectively. In the same binary system, the removal
rates of Cu(II) and Ni(II) are remarkably reduced to 64% and 52%, re-
spectively. In the Cu(II)–Ni(II) system, the removal rates of Cu(II) and
Ni(II) are 76% and 65%, respectively. In the ternary mixed system, the re-
moval rates of Pb(II), Cu(II), and Ni(II) are reduced to 90%, 52%, and 43%,
respectively. In the mixed metal solution, the adsorption capacity of
Fe3O4-ATP/EDTA/CS for Pb(II) decreases slightly, whereas the adsorp-
tion capacity for Cu(II) and Ni(II) decreases substantially. In the case
of multimetal solutions, when metal ions compete for the same adsorp-
tion site of the adsorbent, metal ions with high affinity may replace
other metal ions with weak affinity [56]. The experiments show that
the removal efficiency of Fe3O4-ATP/EDTA/CS for the three metals is
Pb(II) > Cu(II) > Ni(II). This may be due to the smallest hydration radius
of Pb(II) and low mass transfer resistance.
3.11. Adsorption mechanism
XPS characterization of metal ion-loaded adsorbents was conducted
to study the adsorption mechanism of Fe3O4-ATP/EDTA/CS for Cu(II),
Pb(II), and Ni(II). Fig. 13a presents that the characteristic peaks of Cu
(II), Ni(II), and Pb(II) appear at 931.8, 853.2, and 135.2 eV, respectively,
proving that the metal ions are successfully loaded on the adsorbent.
The three peaks in N 1s (Fig. 13b) are attributed to N\\C, −NH/−NH2,
and −NH+ 3 , respectively. After the adsorption of heavy metal ions, the
position of the absorption peak of −NH/−NH2 in Fe3O4-ATP/EDTA/CS
changes, and the other peaks are basically unchanged. In the absorption
peaks of O=C−O−, C–O–C, and C–O–H in O 1s (Fig. 13c), the peak po-
sition of C–O–C remains unchanged, whereas the positions of the two
other peaks change. These results indicate that the −NH/−NH2, O=
C–O−, and C–O–H functional groups in Fe3O4-ATP/EDTA/CS play an im-
portant role in the adsorption process of heavy metal ions.
3.12. Catalytic performance
In addition to heavy metals, there are some organic pollutants in the
wastewater. The Fe3O4-ATP/EDTA/CS material loaded with Cu(II) can
also degrade bisphenol A (BPA) and found that its removal rate was as
high as 98%. In the meantime, the adsorption and catalytic degradation
performance of Fe3O4-ATP/EDTA/CS on BPA has been studied, and found
that the removal rate of BPA was very low (Table 4). Therefore, the
Fe3O4-ATP/EDTA/CS adsorbent can catalytically degrade BPA after
adsorbing heavy metal ions for secondary utilization. Under neutral
conditions, Fe3O4 cannot react with hydrogen peroxide (H2O2), but
the Cu(II)/H2O2 system will produce copper ions (Cu(III)) as the main
oxidant (Fig. 13d).
International Journal of Biological Macromolecules 182 (2021) 1138–1149
Fe3O4-ATP/EDTA/CS + H2O2 Cu(II) loaded Fe3O4-ATP/EDTA/CS + H2O2
98
4. Conclusions
The study successfully prepared a new type of Fe3O4-ATP/EDTA/CS
gel beads by mixing magnetic ATP and CS and using EDTA to
functionalize it through amidation reaction. It exhibits good adsorption
capacity for heavy metal ions. Specifically, its maximum adsorption ca-
pacities for Pb(II), Cu(II), and Ni(II) are 368.32, 267.94, and 220.31 mg
g−1, respectively. In addition, Cu(II) loaded Fe3O4-ATP/EDTA/CS also
showed good catalytic degradation performance for bisphenol A. This
provides richer possibilities for its use in wastewater treatment. All in
all, the gel beads can treat wastewater with complex composition, and
its gel structure is expected to be mass-produced through a peristaltic
pump. In the meantime, Fe3O4-ATP/EDTA/CS gel beads have great po-
tential in the treatment of wastewater due to their magnetic properties,
convenient recycling and good stability.
CRediT authorship contribution statement
Ping Sun: Methodology, Investigation and analysis, Data curation,
Writing-Original draft preparation.
Wei Zhang: Validation.
Binze Zou: Validation.
Xiangyv Wang: Validation.
Lincheng Zhou: Writing- Reviewing and Editing.
Zhengfang Ye: Project administration.
Quanlin Zhao: conceptualization.
Acknowledgement
No funding received.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.ijbiomac.2021.04.132.
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