Sulfhydryl Functionalized Magnetic Chitosan as an Efficient Adsorbent for High-Performance Removal of Cd(II) from Water: Adsorption Isotherms, Kinetic, and Reusability Studies

In this study, dimercaptosuccinic acid-functionalized magnetic chitosan (Fe3O4@CS@DMSA) was synthesized via in situ coprecipitation process and amidation reaction, aiming to eliminate cadmium (Cd(II)) ions from an aqueous environment. The structure, morphology, and particle size of the Fe3O4@CS@DMSA adsorbent were investigated using FTIR, TEM, EDX, TGA, zeta potential, and XRD techniques, and the obtained results approved the successful synthesis of the Fe3O4@CS@DMSA nanocomposite. The influence of external adsorption conditions such as pH solution, adsorbent mass, initial Cd(II) concentration, temperature, and contact time on the adsorption process was successfully achieved. Accordingly, pH: 7.6, contact time: 210 min, and adsorbent mass:10 mg were found to be the optimal conditions for best removal. The adsorption was analyzed using nonlinear isotherm and kinetic models. The outcomes revealed that the adsorption process obeyed the Langmuir and the pseudo-first-order models. The maximum adsorption capacity of Fe3O4@CS@DMSA toward Cd(II) ion was 314.12 mg/g. The adsorption mechanism of Cd(II) on Fe3O4@CS@DMSA nanocomposite is the electrostatic interaction. The reusability test of Fe3O4@CS@DMSA nanocomposite exhibited that the adsorption efficiency was 72% after the 5th cycle. Finally, this research indicates that the Fe3O4@CS@DMSA exhibited excellent characteristics such as high adsorption capacity, effective adsorption-desorption results, and easy magnetic separation and thus could be an effective adsorbent for removing Cd(II) ions from aqueous solutions.


Introduction
Water contamination by a toxic cadmium (Cd(II)) metal is a widespread environmental issue owing to its long-term adverse effects on humans and ecosystems. Cd(II) is one of the most dangerous metal ion due to its nondegradable, strong bioaccumulate, and highly toxic even at low concentrations, which leads to a serious threat to human health [1,2]. Cd(II) pollution can cause kidney, liver, and bone damage to humans with a long time exposure. Cd(II) has excellent solubility which can be easily released into the aqueous systems through industrial production processes such as alkaline batteries, electroplating, textile printing industries, and pigment [3]. Cd(II) is classified as a category one carcinogen by U.S. EPA, and the maximum concentration of Cd(II) in drinking water is 5 μg/L [4,5]. Thus, the removal of extremely toxic cadmium from an aqueous environment is essential to avoid pollution to the environmental systems. Several techniques, namely, chemical precipitation [6], adsorption [7], membrane separation [8], ion exchange [9], and electrodeposition [10,11], have been applied to treat the toxic metals from wastewater. Among them, the adsorption technique has been proven economical, simple, easy operation and ecofriendly, cost-effective, versatile in nature, and highly efficient for metal removal [12].
Many adsorbents have been applied to adsorption of Cd(II) from aqueous medium like sulfonated biochar [13], functionalized cellulose derived [14], amino-functionalized lignin [15], metal-organic framework (MOF) ZIF-8 [16], EDTA/mGO [17], and para-aminobenzoic acid-functionalized activated [18]. These adsorbents suffer from the difficulty of recovering metal after adsorption using traditional methods such as centrifugation and filtration, which may result in secondary pollution and loss of the amount of adsorbents [19]. Magnetic nanocomposite has received great attention as an efficient adsorbent owing to its many advantages such as easy magnetic separation, high surface area, low toxicity, biocompatibility, and the existence of a large number of surface hydroxyl groups that use them in surface modification. To improve the stability of Fe 3 O 4 nanoparticles under acidic conditions and reduce the agglomeration of the nanoparticles, the surface of Fe 3 O 4 nanoparticles can be modified with some materials like activated carbon [20], graphite oxide [21], and carboxylated MNP nanoparticles [22].
Naturally abundant polysaccharides such as chitosan are considered as one of the most promising surface stabilizing materials for magnetite nanoparticles due to their multifunctionality, nontoxicity, biocompatibility, and renewability [23]. Chitosan has a strong affinity with metal ions because of the existence of NH 2 and OH groups which can serve as the active adsorption sites for the removal of metals [24][25][26]. To improve the number of active adsorption sites for adsorption on magnetic chitosan, it needs to be surface modified to provide specific functional groups. Meso-2,3dimercaptosuccinic acid (DMSA) is a suitable candidate for enhancing the adsorption process owing to DMSA having carboxyl and thiol groups, which can be used for the capture of heavy metals [27,28]. In addition, DMSA acid is a nontoxic chelating agent and FDA approved drug which has been used to treat heavy metal poisoning in the human body [29][30][31]. To the best of our knowledge, the Fe 3 O 4 @CS@DMSA nanocomposite has not been used for the elimination of pollutants.
In this study, Fe 3 O 4 @CS@DMSA nanocomposite was synthesized by an in situ coprecipitation method followed by a covalent functionalization of Fe 3 O 4 @CS with DMSA acid via amidation reaction. The synthesized Fe 3 O 4 @CS@DMSA adsorbent was applied to eliminate Cd(II) ions from water. The synthesized Fe 3 O 4 @CS@DMSA was characterized using zeta potential, FTIR, XRD, TGA, TEM, and EDX techniques. The impact of external adsorption conditions such as pH solution, adsorbent mass, initial Cd(II) concentration, temperature, and contact time on the adsorption process was successfully achieved. To achieve the adsorption capacity and mechanisms of Cd(II) adsorption onto Fe 3 O 4 @CS@DMSA nanocomposite, the equilibrium kinetic and isotherm were studied. Thermodynamic parameters were also studied. The reusability test of Fe 3 O 4 @CS@DMSA nanocomposite was performed by carrying out five cycles of adsorption-desorption studies. 2.5. Batch Adsorption Experiments. The removal efficiency of Cd(II) ions by Fe 3 O 4 @CS@DMSA from water was studied by batch method to achieve the impact of various process factors such as adsorbent mass, contact time, pH solution, temperature, and initial Cd(II) concentration on adsorption process. In this work, contact time, solution pH, and adsorbent mass were achieved in the range of 5-350 min, 1.8-9.1, and 5-30 mg whereas temperature and initial Cd(II) concentration were varied from 25 to 45°C and 25 to 300 mg/L. A known amount of Fe 3 O 4 @CS@DMSA was put into an Erlenmeyer containing 25 mL of known Cd(II) concentration, and the sample was then adjusted to the desired pH at 25°C. After that, the sample solution was shaken for 24 h. Then, the sample was isolated by a magnet, and the residual concentration of Cd(II) ions has been determined using AAS. The adsorbed amount (q e (mg/g)) and percentage adsorption of Cd(II) were calculated using Equations (1) and (2), respectively.

Experimental
where C o and C e refer to initial and equilibrium Cd(II) concentration in the solution (mg/L), respectively; V (L) refers to the volume of the Cd(II) solution; m (g) is the weight of Fe 3 O 4 @CS@DMSA nanocomposite. The adsorption capacities for Fe 3 O 4 @CS and Fe 3 O 4 @CS@DMSA adsorbents toward Cd(II) ions were 52.5 mg/g and 58.8 mg/g, respectively, at condition parameters at constant adsorbent mass (0.01 g), initial Cd(II) concentration (25 mg/L), temperature (25°C), pH (7.6), stirring rate (100 rpm), and contact time (1440 min).

Adsorption Science & Technology
to the presence of the ν(-OH) group overlapping with the -NH group. The characteristic band for (-SH) appeared at 2550 cm -1 [34]. Besides, the bands at 1670 and 1554 cm -1 are due to amide I and amide II or δ(N-H) groups, respectively [36], which indicates the formation of amide bonds between Fe 3 O 4 @CS and DMSA [37]. The Fe-O band was decreased to 552 cm −1 , confirming the presence of magnetic nanoparticles. The bands at 1481, 1355, 1274, and 1044 cm -1 are due to ν(-COO-), ν(-C-N), ν(C-O), and ν(O-C-O) stretching vibration, respectively [38,39]. After adsorption of Cd(II), the spectra showed the bands were slightly shifted and decreased in intensity due to the binding of COOH, SH, and OH onto Fe 3 O 4 @CS@DMSA surface with Cd(II) ions through electrostatic attractions. In detail, the bands at 3393 and 2550 cm -1 decrease in intensity owing to the interaction between Cd(II) and carboxyl (COOH), hydroxyl (OH), and SH groups, respectively, on the Fe 3 O 4 @CS@DMSA surface by electrostatic interaction. In addition, the band at 1274 cm -1 for ν(C-O) disappeared after Cd(II) adsorption onto the Fe 3 O 4 @CS@DMSA surface. The decreased intensity of the band at 1481 cm -1 for ν(COO -) indicates the adsorption of Cd(II) onto the Fe 3 O 4 @CS@DMSA surface. Transmittance (%)   Adsorption Science & Technology The XRD patterns of magnetite nanoparticles and Fe 3 O 4 @CS@DMSA are indicated in Figure 1 , (511), and (400) crystal planes of cubic phase magnetite, which was consistent with a previous report [40]. Compared with magnetite, the XRD pattern of Fe 3 O 4 @CS@DMSA appeared a new broad reflection at a 2θ value of 22.5°, confirming the Fe 3 O 4 nanoparticles covered by DMSA and chitosan [41,42]. Using the Scherer equation (3), the average crystal size (D) of Fe 3 O 4 @CS@DMSA nanocomposite was calculated:   [43,44]. The thermal stability of Fe 3 O 4 @CS@DMSA exhibited a high loss in mass of approximately 17% with two stages. In the first one, the weight loss was~3% in low temperature up to 200°C owing to elimination of adsorbed water and solvent absorbed onto the surface Fe 3 O 4 @CS@DMSA nanocomposite. In the second one,~15% weight loss at around 200-700°C ascribes to the thermal decomposition of an organic part of CS and DMSA [45], confirming the successful synthesis of Fe 3 O 4 @CS@DMSA nanocomposites.
To determine the point of zero charge (PZC) of Fe 3 O 4 @CS@DMSA, the surface charge of Fe 3 O 4 @CS@DMSA was measured under different pH values. The outcomes are displayed in Figure 2(b). It was seen that the zero of point charge value (pH pzc ) of Fe 3 O 4 @CS@DMSA nanocomposite was~5.2. This value is lower than~7.1 for Fe 3 O 4 nanoparticles [46]. This behavior of the Fe 3 O 4 @CS@DMSA nanocomposite is mainly assigned to the existence of -OH, COOH, and -SH groups, which are being protonated at lower than~5.2.
The size and morphology of the Fe 3 O 4 @CS@DMSA were studied by TEM, and the outcomes are displayed in . It is clear that the nanoparticles were uniform spherical morphology with a bright of amorphous CS and DMSA over the dark spot crystalline core of magnetite nanoparticles [47]. The value particle size of Fe 3 O 4 @CS@DMSA was~11.5 nm confirming the surface modification of magnetite nanoparticles with CS and DMSA (Figure 3(b) [48]. The effect of different initial pH values (1.8-9.1) on Cd(II) adsorption by Fe 3 O 4 @CS@DMSA nanocomposite was studied as shown in Figure 4(a). The other parameters were kept constant as initial Cd(II) concentration (25 mg/L), temperature (25°C), contact time (210 min), adsorbent mass (10 mg), and agitation speed (100 rpm). As implied in Figure 4(a), the adsorption capacity of Fe 3 O 4 @CS@DMSA toward Cd(II) was increased from 0.75 to 58.75 mg/g as the pH increased from 1.8 to 7.6, respectively. After that, it is slightly reduced and may be owing to the formation of Cd(II) hydroxide precipitate such as Cd(OH) + and Cd(OH) 2 ,   (1)) [38,52]. After the adsorbent mass of 10 mg, no significant change in adsorption capacity was observed.

Effect of Contact Time.
To find out the optimum contact time, experiments were conducted at various time intervals between 5 and 350 min at constant adsorbent mass (10 mg), initial Cd(II) concentration (25 mg/L), pH (7.6), stirring rate (100 rpm), and temperature (25°C) as presented in Figure 4(c). It was noticed that the amount of Cd(II) adsorbed onto the Fe 3 O 4 @CS@DMSA increased rapidly with increasing equilibrium time and the maximum adsorption capacity and removal efficiency reached up to 58.0 mg/g and 92.8%, respectively, at 210 min. In the initial stage of the adsorption process, the Cd(II) ions easily interacted with active sites of Fe 3 O 4 @CS@DMSA nanocomposite owing to the abundance of the active adsorption sites on the Fe 3 O 4 @CS@DMSA surface. After 210 min, no significant change in the adsorption capacity owing to the active sites of Fe 3 O 4 @CS@DMSA tended to saturate and could not easily adsorb the Cd(II) ions. to 295 mg/g with the rising initial Cd(II) ion concentration from 25 to 300 mg/L at 298 K. This phenomenon can be explained that a higher Cd(II) concentration rises the driving force and provides more collisions between Cd(II) ions and active sites of Fe 3 O 4 @CS@DMSA which could improve the adsorption rate. The influence of temperature on the adsorption process is presented in Figure 4(b). The adsorption capacity of Fe 3 O 4 @CS@DMSA toward Cd(II) was decreased from 295 to 195 mg/g when the temperature was improved from 298 K to 318 K at 300 mg/L, suggesting that the adsorption of Cd(II) on Fe 3 O 4 @CS@DMSA is exothermic. This could be explained by the weakening of the adsorptive forces between the active sites of Fe 3 O 4 @CS@DMSA nanocomposite and the Cd(II) ions [53], which is consistent with the previous report on Cd(II) adsorption by MGO-Trp [54] and CSAP [55].
where C e (mg/g) is the equilibrium aqueous-phase Cd(II) concentration. q e and q m refer to the equilibrium and maximum amount of Cd(II) adsorbed (mg/g), respectively; K DR (mol 2 /kJ 2 ), K F , and K L are the constants of D-R, Freundlich, and Langmuir models, respectively; E (kJ/mol) and ɛ are the average free energy and the Polanyi potential, respectively; n is the adsorption intensity. Figure 5 displays the three nonlinear fitting parameter results of the adsorption isotherm models for the Cd(II) adsorption on Fe 3 O 4 @CS@DMSA nanocomposite. By comparison, it was observed that the R 2 values were 0.96215, 0.97072, and 0.7983 for Langmuir, Freundlich, and D-R isotherms, respectively. Thus, the experimental data was better described by the Freundlich (R 2 = 0:97072) model than those of the Langmuir and D-R models, which indicated the heterogeneous nature of Fe 3 O 4 @CS@DMSA and a contribution of electrostatic interaction to the Cd(II) adsorption on Fe 3 O 4 @CS@DMSA (physisorption nature) [59]. By applying the Freundlich equation, the values of n (adsorption intensity) were in the range of 2.2381-3.2730, indicating that multilayer adsorption occurred onto the heterogeneous surface of Fe 3 O 4 @CS@DMSA. In addition, the Cd(II) adsorption is a favorable process. The higher value of n = 3:2730 at 298 K indicates that the Fe 3 O 4 @CS@DMSA nanocomposite has better adsorption performance [59,60]. According to the Langmuir model, the maximum amount of Cd(II) adsorbed was 314.12 mg/g. This value is higher than other material adsorbents for adsorption of Cd(II) like Fe 3 O 4 /chitosan-glycine-PEGDE (171.06) [61], polyethyleneimine-modified magnetic porous cassava (143.6) [62], chitosan-modified kiwi branch biochar (126.58) [63], sulfhydryl-modified chitosan beads (183.1) [64], MNP-DMSA (25.44) [65], chitosanpectin gel beads (177.6) [66], chitosan-iron oxide (CS-Fe 2 O 3 ) (204.318) [67], and thiocarbohydrazide-chitosan gel (81.26) [68] (Table 3). According to the D-R isotherm, the values of means free energy (E) were found to be in the range of 0.0396-0.1773 kJ/mol), which indicated that the Cd(II) adsorption onto Fe 3 O 4 @CS@DMSA nanocomposite classified as a physical adsorption process due to the E value is less than 8 kJ/mol [69].
q t = q 2 e k 2 t 1 + q e k 2 t , ð11Þ

Adsorption Science & Technology
where q e and q t (mg/g) refer to the amounts of Cd(II) adsorbed on Fe 3 O 4 @CS@DMSA at equilibrium and time t, respectively; k 1 is the PFO rate constant; k 2 represents the PSO rate constant; β (mg/g) is the Elovich kinetic parameter; α refers to the desorption constant.
Based on R 2 values, PFO displays a better correlation coefficient (R 2 = 0:97515) than the PSO (R 2 = 0:9567) and Elovich (R 2 = 0:93427) models, suggesting the rate-limiting step for Cd(II) is physisorption involving electrostatic interaction between Cd(II) and Fe 3 O 4 @CS@DMSA nanocomposite. The value of q e:cal (61.45 mg/g) calculated is close to the experimental equilibrium adsorption capacities (q e,exp = 58:75 mg/g). By applying the Elovich equation, the values of α and β were 0.877 mg/g min and 0.043 mg/g with R 2 (0.93427), respectively. The low value of R 2 indicates the absence of a chemisorption mechanism.
3.3.3. Adsorption Thermodynamics. The thermodynamic parameters, namely, enthalpy change (ΔH°) (Equation (12) and entropy change (ΔS°) (Equation (12)), can be obtained from the slope and intercept of the Van't Hoff plot of ln K e vs. 1/T (Figure 6(a)) at different temperatures (298-318 K), and the free energy change (ΔG°) can be estimated from the equation (Equation (13)): where K 0 e (Equation (14)) is the thermodynamic equilibrium constant at a certain temperature [59][60][61] and [adsorbate]°, γ, and K L are the standard concentrations of the adsorbate (1.0 mol/L), activity coefficient, and Langmuir constant, respectively. The thermodynamic parameters for Cd(II) adsorption onto Fe 3 O 4 @CS@DMSA are summarized in Table 5. The negative values of free energy (ΔG°) was noticed, indicating that the Cd(II) adsorption onto Fe 3 O 4 @CS@DMSA is a spontaneous reaction and the values of ΔG°were increased from -22.36 to -19.66 kJ/mol with rising temperature from 298 to 318 K which demonstrates the favorability of the adsorption of Cd(II) at a lower temperature. Negative values of ΔH°and ΔS°indicated that the Cd(II) adsorption onto Fe 3 O 4 @CS@DMSA was exothermic and the decreased the reaction randomness. Figure 7. Based on the adsorption kinetic results, the adsorption process followed the pseudo-firstorder model, suggesting a physical interaction through electrostatic attraction between the Cd(II) ions and the Fe 3 O 4 @CS@DMSA nanocomposite. According to the FTIR analysis (Figure 1(a)), the position peaks of functional groups declined in intensity and slightly shifted to a lower wavenumber. In detail, the bands at 3393 and 2550 cm -1 decrease in intensity owing to the interaction between Cd(II) and carboxyl (COOH), hydroxyl (OH), and SH groups, respectively, on the Fe 3 O 4 @CS@DMSA surface by electrostatic interaction. In addition, the band at 1274 cm -1 for ν (C-O) disappeared after Cd(II) adsorption onto the Fe 3 O 4 @CS@DMSA surface. The decreased intensity of the band at 1481 cm -1 for ν(COO -) indicates the adsorption of Cd(II) onto the Fe 3 O 4 @CS@DMSA surface. Besides, the  (15)) was estimated by the equation:

Adsorption Mechanism. The proposed adsorption mechanism is shown in
where C m and C e (mg/L) refer to the concentration of Cd(II) ion released in the solution and the initially adsorbed Cd(II) concentration, respectively. The results of the Cd(II) adsorption/desorption test on Fe 3 O 4 @CS@DMSA nanocomposite using eluents are indicated in Figure 6(b). It was observed that the percentage desorption was found to be CH 3 COOH (47.48%), HNO 3 (87.26%), and HCl (91.3%), which indicate the best eluent for desorption of Cd(II) was 0.01 M HCl owing to the smaller ionic size of the Clion compared to CH 3 COOand NO 3 -. For reusability of the Fe 3 O 4 @CS@DMSA study, the Cd(II)-loaded Fe 3 O 4 @CS@DMSA was isolated using a magnet and then the solid adsorbent was washed with deionized water, dried, and regenerated with 25 mL of 0.01 M HCl. After that, the sample was shaken at room temperature for 210 min. The solid/solution phase is separated via a magnet, and the supernatants are analyzed by the AAS method. After desorption, the Fe 3 O 4 @CS@DMSA nanocomposite was reused to Cd(II) adsorption and five adsorption/desorption cycles were applied. The results obtained are presented in Figure 6(c). It is seen that up to five cycles about 72% of Cd(II) were successfully removed. The reduction in removal efficiency of Cd(II) after five cycles may be owing to incomplete desorption of the Cd(II) ions on Fe 3 O 4 @CS@DMSA.

Conclusion
Fe 3 O 4 @CS@DMSA nanocomposite was synthesized via the in situ coprecipitation method followed by a covalent functionalization of Fe 3 O 4 @CS with DMSA acid by amidation reaction. The synthesized Fe 3 O 4 @CS@DMSA nanocomposite was characterized using zeta potential, FTIR, XRD, TEM, EDX, and TGA techniques. These techniques confirmed the formation of adsorbent successfully. After characterization, the Fe 3 O 4 @CS@DMSA was used to eliminate Cd(II) ions from aqueous systems. The Fe 3 O 4 @CS@DMSA adsorbent exhibited a high adsorption capacity (314.12 mg/g at the optimum condition pH: 7.6, contact time: 210 min, temperature: 298 K, adsorbent mass:10 mg, and stirring rate: 100 rpm). The FTIR and EDX results confirmed the existence of Cd(II) ions after adsorption on Fe 3 O 4 @CS@DMSA nanocomposite. The Freundlich isotherm data and pseudofirst-order kinetic data displayed more compatibility with the equilibrium data than that of other models. The mecha-nism of Cd(II) adsorption on Fe 3 O 4 @CS@DMSA nanocomposite is electrostatic attraction. The thermodynamic results confirmed the spontaneous and exothermic nature of adsorption. The reusability test of Fe 3 O 4 @CS@DMSA nanocomposite exhibited that the adsorption efficiency was 72% after five cycles. The results indicate that the Fe 3 O 4 @CS@DMSA has a good potential for the elimination of Cd(II) from an aqueous solution.

Data Availability
Anyone who wants to request research article data can contact me directly via the following email: aalkudami@ksu.edu.sa, aaaayoub17@gmail.com, Chemistry Department, College of Science, King Saud University.

Conflicts of Interest
There are no conflicts to declare.