Adsorption of Pb(II) from aqueous solution using a

International Journal of Biological Macromolecules 115 (2018) 1142–1150

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International Journal of Biological Macromolecules journal homepage: http://www.elsevier.com/locate/ijbiomac

Adsorption of Pb(II) from aqueous solution using a magnetic chitosan/graphene oxide composite and its toxicity studies Melvin S. Samuel a, Sk. Sheriff Shah b, Jayanta Bhattacharya a, Kalidass Subramaniam c, N.D. Pradeep Singh b,⁎ a b c

School of Environmental Science and Engineering, Indian Institute of Technology, Kharagpur, West Bengal 721302, India Department of Chemistry, Indian Institute of Technology, Kharagpur, West Bengal 721302, India Department of Animal Sciences, Manonmaniam Sundaranar University, Thirunelveli 627012, Tamil Nadu, India

a r t i c l e

i n f o

Article history: Received 18 February 2018 Received in revised form 5 April 2018 Accepted 30 April 2018 Available online 02 May 2018 Keywords: MCGO composite material Adsorption A549 cells

a b s t r a c t This study involves the adsorption of lead using magnetic chitosan/graphene oxide (MCGO) composite material in batch mode. The MCGO composite material was synthesized via modified Hummers method. The MCGO composite material was characterized by powder x-ray diffraction (PXRD), Fourier transform infrared spectroscopy (FT-IR), scanning electron microscopy (SEM), Tunnelling electron microscopy (TEM), thermogravimetric analysis (TGA), Brunauer–Emmett–Teller (BET) and UV–vis diffusive reflectance spectra. The adsorption mechanism of MCGO composite material was well described by Langmuir isotherm and pseudo second order kinetic model, with a high regression coefficient (b0.99). The MCGO composite material was applied for the removal of lead metal from aqueous solution. We have also evaluated toxicity of synthesized MCGO composite material by examining on A549 cells. The results have shown that MCGO material showed viable cell percentage of 53.7% at 50 μg and 44.8% at 100 μg. © 2018 Elsevier B.V. All rights reserved.

1. Introduction Global scenario of heavy metals pollution has become a concern due to their higher toxicities and it accumulates in humans via food chain. These heavy metals are non-biodegradable and carcinogen to humans. Lead, mercury, chromium, arsenic, cadmium, zinc, copper and nickel are the most common contaminants found in contaminated surface water and groundwater as well as industrial wastewater. The occurrence of these heavy metals in water causes great threats to humans and other living organisms [1–3]. Lead (Pb) is a common heavy metal pollutant that is more prevalent in the industrial waste water. This Pb is non-biodegradable and hence it can cause serious health hazards to living organisms initiating renal impairment, anaemia, haemolysis, liver disfunction and neuronal cell injury [4]. According to world Health Organisation (WHO) and US Environmental Protection Agency (US EPA) have set the permissible limit for lead in drinking water to be 0.01 and 0.015 mg/L. The tolerance limit of other metals such chromium, manganese, arsenic, nickel and copper have set the permissible limit in drinking water to be lesser than 0.20 mg/L [5]. As heavy metals are non-biodegradable, clean-up of contaminated water and soil is rather challenging. The available technologies that are reported for the lead removal includes chemical precipitation, ion exchange, reduction, electrochemical precipitation, solvent extraction, membrane ⁎ Corresponding author. E-mail address: [email protected] (N.D. Pradeep Singh).

https://doi.org/10.1016/j.ijbiomac.2018.04.185 0141-8130/© 2018 Elsevier B.V. All rights reserved.

separation, cementation, evaporation and foam formation. However, high energy and chemical requirement, incomplete removals, generation of secondary pollution, toxic sludge are the limiting factors of these treatment procedures [6,7]. It is indeed urgent to develop costeffective technologies that can effectively remove the heavy metals from contaminated water. Iron oxide are generally magnetite (Fe3O4), maghemite (Fe2O3), hematite (Fe2O3) and goethite (FeO(OH)). Among the above mentioned iron oxides, magnetite and maghemite exhibit magnetic nature [8]. The presence of Fe3O4 in the adsorbent material provides an additional stability, decrease toxicity and repeated reusability of the adsorbent is possible [9]. This magnetic nanoparticles (MNPs) are available at low cost and provides other advantageous reasons such as lack of internal diffusion resistance and it provides a high surface to volume ratio. Hence this material can be used in the field of environmental, medical and chemical engineering. Graphene is a carbon material with oneatom thickness and honeycomb structure. This fascinating material is attributed to its excellent mechanical and physicochemical properties [10]. In recent years graphene oxide (GO) is being considered has a superior adsorbent for adsorbing the heavy metal ions than the existing adsorbents used for water treatment. The GO contains very high specific surface area, widespread functional groups and thereby it enhances their reactivity [11,12]. Based on favourable adsorption properties, some researchers have coupled chitosan-GO composite for adsorption studies [13]. The magnetic chitosan/graphene oxide composite was used for adsorption of methylene blue [14]. Graphene oxide-MnFe2O4

M.S. Samuel et al. / International Journal of Biological Macromolecules 115 (2018) 1142–1150

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was then stirred at 50 °C in water bath for 24 h. During this reaction, the color of the mixture varied from black to brown. Then 150 mL of water was added slowly to the mixture with ice bath. In this reaction a large amount of heat was released due to the addition of water in to the concentrated H2SO4. Followed by addition of 50 mL of 30% H2O2 under stirring condition and thereby the color of the mixture turns yellow with bubbling. The mixture was then centrifuged and washed with 15% HCl, ethanol and water, the pH was adjusted to 7. The final sample was dried in 40 °C for 72 h.

magnetic nanohybrids for removal of lead and arsenic [15]. The polymer based graphene oxide magnetic nano-sorbent for the removal of Pb(II) [16]. Sodium modified reduced graphene oxide-Fe3O4 nanocomposite for efficient lead (II) adsorption [17]. Incorporation of Graphene oxide into Chitosan Poly(acrylic acid) porous polymer nanocomposite for enhanced lead adsorption [18]. The water-dispersible magnetic chitosan/ graphene oxide composites for selective adsorption of lead ions [19]. Magnetic chitosan lignosulfonate grafted with graphene oxide for decontamination of methylene blue [20]. Magnetic composite of activated carbon and superparamagnetic Fe3O4 nanoparticles [21]. GO exhibit hydrophilic nature, which remains well-dispersed and suspended in water. The major limitations of this GO are (a) recovery from any aqueous solution is a tedious process; (b) filtration; (c) centrifugation; (d) causes turbidity in effluent. In order to circumvent the limitation of GO we have incorporated ferrate magnetic material (Fe3O4) nanoparticle. Where the carboxyl group of GO chemically reacts with the Fe3O4 nanoparticle. In this study, we have reported that developed MCGO composite material for adsorption of Pb(II). The developed MCGO material offers a large specific area, abundant surface groups and high portion of sp2 carbon region, this can enhance the adsorption capacity as well it can immobilize and well disperse the GO. The aim of the study was to examine the adsorptive potential of MCGO composite material on lead. This new type of MCGO composite material, featuring extraordinary adaptability, low cost, easy operation and explicit regeneration will be a useful technique for the removal of heavy metal from waste water. Additionally we have also performed cell viability assay with A549 cell line with respect to GO, Fe3O4 and MCGO materials.

The prepared GO (0.1 g) was dispersed in 100 mL distilled water by sonication for 5 h followed by the addition of 5 g chitosan (CS) powder and 2 g of sodium borohydride (NaBH4). The suspension was heated and refluxed at 100 °C for 4 h. The reaction mixture was then filtered and the obtained CS-GO was washed with distilled water and dried at room temperature 27 °C. This CS-GO adsorbent material was used for further experiments. The synthesis of GO/chitosan/Fe3O4 followed a slightly modified hydrothermal approach. FeCl3.6H2O (2.03 g), FeCl2.4H2O (0.7 g) and CS-GO (1.35 g) were added to round–bottom glass vessel and the solution was continuously stirred and heated at 50 °C for few minutes. To this 8 M NaOH heated to the same temperature was added slowly (under continuous stirring). The reaction was continued for 15 min and then cooled down to room temperature. The obtained blackish precipitates were magnetically separated and washed with excess of water to remove the unbound particles. Finally, the precipitates were dried at room temperature for 24 h.

2. Materials and methods

2.5. Analytical method

2.1. Materials

A stock solution of Pb(II) (1000 mg/L) was prepared by dissolving the appropriate amount of lead nitrate (Pb(NO3)2) in distilled water. Further, the Pb(II) concentrations (0–150 mg/L) were prepared by diluting the stock solution with distilled water and the pH was adjusted to 5. After adsorption using the MCGO composite material the left out Pb(II) concentrations in the samples were evaluated using atomic absorption spectroscopy (AAS, Shimadzu AA 6800) at wavelength 283.3 nm. The lamp current and slit width was 13 mA and 0.5 nm respectively. Air/acetylene flame was used for all the experiments. The calibration curve was made with a standard solution within a linear range and a high correlation coefficient (R2 N 0.99). The adsorption capacity and removal efficiency of Pb(II) adsorbed on adsorbents was calculated by the following equation.

The graphite powder (99.0%), iron (III) chloride hexahydrate (FeCl3·6H2O), iron (II) chloride tetrahydrate (FeCl2·4H2O), potassium permanganate (KMnO4), sulfuric acid (H2SO4), sodium nitrate (NaNO3), hydrochloric acid (HCl), sodium hydroxide (NaOH) was purchased from Sigma Aldrich, Bangalore (India). 2.2. Instrumentation and characterization The powder X-ray diffraction patterns (PXRD) were recorded on a PANalytical X'pert PRO diffractometer and samples were scanned from 5 to 80° (2Ɵ). Fourier transform infrared (FTIR) spectra were recorded on a Nicolet NEXUS 470-FTIR spectrophotometer as KBr pellets. Scanning electron microscopy (SEM) images were collected using a Zeiss Auriga instrument. TEM was done to reveal the morphology and particle size of the GO and MCGO composite material (Model: FEI-TECHNAIG2 20 TWIN). Surface area and micro pore volume of the samples were measured by N2 adsorption isotherm using an ASAP 2010 Micromeritics instrument by Brunauer–Emmett–Teller (BET) method. TGA measurements were conducted with a heating rate of 10 °C/min under nitrogen atmosphere at the temperature ranging from 50 to 800 °C. TGA curves were recorded with a thermo-gravimetric and differential thermal analyzer (Perkin Elmer Inc., Massachusetts, USA). For analyzing Pb(II) concentration, a PerkinElmer Analyst 700 flame atomic absorption spectrometer (AAS) with deuterium background corrector was used. 2.3. Preparation of graphene oxide GO was prepared from commercially available graphite powder using modified Hummers method. To the 3 g of graphite powder, concentrated H2SO4 (70 mL) and H3PO4 (100 mL) was added with an ice bath. Under continuous stirring, 9 g of KMnO4 was added slowly and the temperature of the reactant was kept at 4 °C for 1 h. The mixture

2.4. Synthesis of MCGO

qe ¼

C o −C f V M

%removal ¼

C o −C f 100‘ Co

ð1Þ

ð2Þ

where Co and Cf are the initial and equilibrium concentration of Pb(II) respectively. V(L) is the volume of the solution, M(g) is the weight of the adsorbent and qe (mg/g) is the adsorption capacity of the adsorbent. The impact of pH in the adsorption of Pb(II) was evaluated at the pH range of 1.0–10.0. The adsorption experiments were carried out for 24 h in 20 mL glass vials containing 10 mL Pb(II) solution (50 mg/L). The optimized amount of adsorbent was determined by varying the MCGO composite material from 0.5–2 g/L of 50 mg/L Pb(II) solution and contact time for 24 h. The kinetic studies were carried out by adding 1 g/L MCGO composite material to 50 mg/L of Pb(II). At predetermined time (0–600 min), from which 0.5 mL aliquots were withdrawn and analysed for residual Pb(II) concentrations. The rate of adsorption was determined by pseudo first order, pseudo second order and intra-particle diffusion. The adsorption equilibrium studies were carried out by adding 1 g/L MCGO composite material to 10 mL of Pb(II) solution at initial

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concentration varying from 10 to 150 mg/L and kept for 24 h contact time. Langmuir and Freundlich isotherm models were applied for evaluating the adsorption process.

The percentage of viable cells was calculated using the formula, Viable cells percentage ¼

Control OD−Test OD 100 Control OD

2.6. Desorption and reusability The reusability experiments were conducted on MCGO composite material using four adsorption-desorption cycles. For each adsorption cycle, 1 g/L MCGO composite materials were used for 10 mL of 50 mg/L Pb(II) solution and MCGO composite material were shaken for 24 h at 27 °C. The solution was filtered to collect the Pb(II) loaded MCGO composite material and the attained Pb(II) loaded MCGO composite material was added to 0.1 M HCl solutions, shaking (120 rpm) at 27 °C for 3 h. The obtained MCGO composite material was washed with water and dried at 65 °C for successive cycles. The adsorptiondesorption cycle was repeated for 4 times by the spent MCGO composite material. 2.7. Cell culture Lung cancer cell line A549 procured from NCCS, Pune, India. This A549 cell were cultured in F-12K culture medium supplemented with 10% (v/v) fetal bovine serum and incubated at 37 °C in a 5% CO2/95% air. 2.8. Cell morphology A549 cell line revived from glycerol stock and passaged until the cells acquire 80–90% confluency. After subsequent splitting and passaging, cells were placed in the 96-well plates and 1 × 106 cells per well were seeded in each well and incubated for 24 h (37 °C and 5% CO2). The MCGO composite material was introduced separately to cells with a pre-fixed concentration in culture medium. Cells without materials were taken as control. 2.9. Cell viability The cell viability and the toxicity were examined on A549 cell. The MCGO composite material concentration range varied from 50 to 250 μg respectively. Each test sample dissolved in DMSO and further diluted with culture medium DMEM (Dulbecco minimal essential medium) containing 10% FBS to obtain the respective concentrations. The DMSO concentration was kept b1% in the culture medium. A549 cells 1 × 106 cells/well incubated with test sample at 37 °C under 5% CO2 atmosphere for 48 h followed by addition of MTT and further incubation for 4 h. The resultant blue farmazane was dissolved in DMSO. The cytotoxicity was evaluated with the absorption at 570 nm with an ELISA reader.

3. Results and discussion 3.1. Adsorbent characterization The synthesized GO sheets were found to be greater than the pristine graphene sheets [22]. The MCGO composite material were prepared for Pb(II) adsorption. The graphene oxide (GO) nano-sheets were synthesized according to Hummers method. The average size of the MCGO composite material was found to be 200 nm by TEM. 3.1.1. Surface morphology The surface morphologies of the GO and MCGO composite material are shown in Fig. 1. Here the GO material shows a regular external surface, with roughness and has some cavities and these cavities are relatively distributed uniformly on the GO adsorbent surface (Fig. 1a). Whereas the MCGO composite adsorbent material shows a rough external surface, with irregular colonies and no visibility of cavities are seen. This must be due to the attachment of the ferrite nanoparticle and chitosan on to the surface of the adsorbent material (Fig. 1b). To further validate the morphology of the MCGO composite material SEM analysis was performed. The SEM images of GO, Fe3O4 and MCGO composite material before and after adsorption are shown in Fig. 2a–d, respectively. 3.1.2. Fourier transform infrared spectroscopy The FTIR pattern of GO shown the characteristic peaks at 3302 cm−1 (OH stretching vibrations), 1734 cm−1 (C_O stretching carbonyl and carboxyl group), 1624 cm−1 (CC stretching vibrations), 1058 cm−1 (CO stretching vibration of epoxide) were observed (Fig. 3a). Whereas, the FTIR spectrum of synthesized MCGO composite material differed from that of GO is evident by the weakening of the peaks 3302 cm−1. Which implies that the \\OH groups are also involved in hydrogen bonding with the chitosan molecules. In the synthesized MCGO composite material, the COOH peak of GO at 1734 cm−1 has completely disappeared. The band at 578 cm−1 in MCGO composite material was attributed to Fe3O4, thereby it confirms the presence of Fe3O4. 3.1.3. Powder X-ray diffraction (PXRD) The XRD spectra of GO and MCGO composite material are shown in Fig. 3b. The characteristic peak for GO appeared at 2Ɵ = 9.56°. Similarly, the diffraction pattern for Fe3O4 nanoparticle appeared at 2Ɵ = 30.2°,

Fig. 1. TEM images of materials (a) GO, (b) MCGO composite material.


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Fig. 2. SEM images of materials (a) GO, (b) Fe3O4, (c) MCGO before Pb(II) adsorption, (d) MCGO after adsorption.

35.6°, 43.3°, 53.7°, 57.3° and 62.8°, which corresponds to (220), (311), (222), (400), (422), (511), and (440) Bragg reflection, respectively [23]. The planes of crystal iron oxide were further confirmed using standard powder diffraction data of the Joint Committee on Powder Diffraction Standards (JCPDS no. 19–0629) signifies the presence of magnetic oxide. All peaks corresponded to a face centered cubic (fcc) symmetry [24,25]. Whereas, MCGO composite material exhibited a broad peak at 2Ɵ = 9.56°, 20.07°, indicating the presence of GO and Fe3O4 nanoparticle moiety. The MCGO composite material exhibited a sharp peaks of both GO and Fe3O4 nanoparticle. 3.1.4. Thermogravimetric analysis The TGA analysis was done for the prepared GO and MCGO composite material, the curves were recorded in N2 atmosphere are shown in Fig. S1a and b†. The GO exhibited reduction in mass upon heating above 100 °C, this might be due to adsorbed water molecules [30]. The GO (curve a) The GO showed two major weight losses. The first weight step, started at above 80 °C was observed, this might be due to vaporization of the adsorbed water molecules on GO sheets. While the second weight loss step, occurs at about 200 °C, these are actually assigned to the elimination of oxygenated functional groups of GO (i.e. C_O, C\\O\\C and\\OH). Similarly, there occurs a weaker mass loss in the range of 320 to 600 °C is related to the elimination of more stable functional groups. Whereas the MCGO material (curve b) showed better stability than the GO material and here the main weight loss occurs in the range of 280 °C and 530 °C. Based on TGA data, the MCGO material exhibits relatively higher thermal stability than GO sample. 3.1.5. Specific surface area and porous structure of MCGO material The specific surface area and porous structure of MCGO material were determined by nitrogen adsorption-desorption isotherms. Brnauer-Emmett-Teller (BET) showed cumulative pore volume (Pvol - 0.0899 cm3/g), average pore diameter (Pdiam – 68.75 Å), pore

size (Psize - 56.76 Å) and specific area for the MCGO composite material was 74.345 m2/g. The isotherm curve pattern exhibited a steep increase at low relative pressure indicating the microporous characteristics, the broad hysteresis loop in the medium relative pressure range, signifying the formation of mesoporous structure. Similarly, the total pore volume and pore size distribution were calculated by Barrett-Joyer-Halenda (BJH) model from the nitrogen adsorption isotherm are shown in Fig. S2a and b†. 3.1.6. Optical properties To investigate the conductivity of MCGO composite material, the diffusive reflectance for powder sample was carried out to obtain band gap (Eg). UV–vis diffusive reflectance spectra of MCGO composite material in the range of 200–800 nm are shown in Fig. 3†. The band gap energy of MCGO composite material was calculated using Tauc's relation equation.

αhv ¼ A hv−Eg

n

where, α – absorption coefficient, hυ – discrete photo energy, A constant, Eg – band gap. Exponential n denotes the type of transition, n = 2 for the direct transition. The band gap of MCGO catalyst material is 2.26 eV. The band gap energy values of MCGO composite material is shown in Fig. S3b†. 3.2. Removal of Pb(II) ions by the MCGO composite material A preliminary study was conducted using MCGO composite material interacting with lead solution (50 mg/L) with adsorbent material (1 g/L) at pH-5.

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Fig. 3. a. FT-IR spectrum of (a) GO. (b) MCGO; 3b. XRD patterns of (a) GO, (b) Fe3O4, (c) MCGO.

3.2.1. Effect of pH The pH value is the prime factor for metal adsorption on the adsorbent. The pH plays a significant effect on the surface charge of the adsorbents and degree of ionization. In most of the cases the adsorption processes do not occur at low pH, since the adsorption process of metal ions is pH sensitive. Henceforth, a wide range of pH was chosen from 1.0 to 10.0 to determine the effect of pH and the results are shown in Fig. 4. From the result it was evident that upon increasing the pH from 1.0 to 5.0, the adsorption capacity for Pb(II) increased

Fig. 4. Effect of pH on the adsorption of Pb(II) on MCGO material.

sharply. This is mainly because the adsorbent material contains a lot of free sites such as \\COO− and \\O− and these functional groups gets protonated at low pH and thereby resulting in decreased adsorption. While increase in pH, results showed increased adsorption of Pb(II) ions, this is due to the availability of more sites on the adsorbent. Here, 92% of Pb(II) ions were removed from the solution at pH 5. Hence, pH 5 was chosen as the optimum pH for further experimental trials. Temperature: The effect of temperature on Pb(II) adsorption was examined with four different temperatures (20, 27, 35 and 42 °C). It was evident that the removal percentage of Pb(II) ions increases from 65% at 20 °C to 92% at 27 °C. To determine the point of zero charge of the adsorbent, pHpzc, 1.0 g/L, MCGO material was added to 20 mL of 0.01 M NaCl solution. The pH values of the solutions were adjusted with HCl or NaOH to 1, 3, 5, 7, and 9. The samples were stirred at 120 rpm for 24 h. The pH values of the solutions were measured after removing the adsorbent material. The pHpzc value was determined by using a plot which displays the final pH versus initial pH. These results are presented in Fig. S4†. The pHpzc values were determined as 8, where no difference between initial and final pH values observed. The impact of interfering NaCl on lead (Pb(II)) ion removal from aqueous solutions containing initial Pb(II) ion concentration of 50 mg/L onto MCGO composite material was studied. The results have shown that the presence of NaCl had only meager effect on the uptake capacity of Pb(II). The obtained results are in agreement with earlier study report [26]. 3.2.2. Effect of contact time The effect of contact time on the uptake of Pb(II) by MCGO composite material is shown in Fig. 5. The figure shows, the graph of percentage removal (Fig. 5a) and uptake capacity (Fig. 5b) obtained at different concentrations with change in time. The effect of contact time on the


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Fig. 5. Effect of contact time on the (a) % removal and (b) capacity (mg/g) of Pb(II) on MCGO composite material.

removal of Pb(II) by MCGO composite material was investigated at three different Pb(II) concentrations (25, 50 and 100 mg/L). Time chosen for this study was 0–600 min with the dose of 1 g/L at temperature 27 °C and agitation speed of 120 rpm. At lower concentrations (b50 mg/L) the maximum Pb(II) adsorption occurred within 420 min, showing 92% removal. It was found that the amount of Pb(II) adsorbed onto MCGO composite material increases with the increase of contact time, this is mainly due to the availability large number vacant sites for adsorption. After the 420 min the adsorption capacity of MCGO composite material reaches equilibrium state. Increase in time beyond 420 min, the amount of adsorption remains same without any significant change due to the non-availability of active site for Pb(II) ions to get adsorbed. Therefore, from the above mentioned results 420 min was selected as the optimal contact time for the further experiments.

3.2.3. Effect of shaking speed The effect of agitation speed on the removal of Pb(II) by MCGO composite material was studied by shaking the 50 mg/L of Pb(II) sample (10 mL) at different shaking speeds viz., 80, 100, 120 and 150 rpm. The other parameters such as pH (5.0), incubation time (420 min) and temperature (27 °C) were kept constant. The result shown that an increase in shaking speed from 80 to 150 rpm, the removal of Pb(II) also increases as shown in Fig. 6.

3.2.4. Kinetic and adsorption isotherm The kinetic models parameters of Pb(II) adsorption onto MCGO composite material are listed in Table 1. The kinetic study was performed to understand the adsorption behaviour of the MCGO composite material shown in Fig. 7. The models such as pseudo-first order, pseudosecond order and intra particle diffusion were validated based on the correlation coefficient (R2). In comparison to the other models, the pseudo-second order model was a best fit. It also showed relatively higher correlation coefficient (R2 = 0.987) and the calculated qe (24 mg/g) is in strong conformity with the experimental qe (24 mg/g) value. Hence, this model suggests that the concentration of adsorbent and adsorbate are associated with the rate determining step of the adsorption process. From the obtained results it could be inferred that the predominant process is chemisorption, which involves sharing of electrons between Pb(II) ions and MCGO composite adsorbent binding sites [1,10]. Generally, the adsorption of Pb(II) ions onto the outer surface of the adsorbent may result in rate limiting step, this is because the transfer of Pb(II) ions from the solution phase into the pores of the adsorbent in the batch mode of experiments. The low R2 value of the intraparticle diffusion model states that the pore diffusion is not the rate-limiting step. The adsorption isotherm studies were performed with an initial concentration Pb(II) concentration of 0–150 mg/L, pH 5, with different adsorbent dosage 0.25, 0.5, 1.0 and 2.0 g/L for 420 min at 27 °C are shown in Fig. 8. The isotherm parameters of the adsorption process were calculated and given in Table 2. Two isotherm models viz Langmuir and Freundlich were used for studying adsorption process. In which the values of the regression coefficients of the Langmuir isotherm model was found to be higher compared to Freundlich model. The

Table 1 Kinetics parameters for the adsorption of Pb(II) by MCGO composite material based on different concentrations.

Fig. 6. Effect of shaking speed on the adsorption of Pb(II) on MCGO composite material.

Concentration (mg/L)

25

50

100

Pseudo first order K1 (min−1) qe (mg/g) R2

8.06 × 10−3 7.84 0.8002

0.0103 101.97 0.6808

8.29 × 10−3 54.51 0.874

Pseudo second order K2 (min−1) qe (mg/g) R2

0.0342 24.64 0.987

0.0237 49.261 0.9904

0.049 65.789 0.9981

Intra-particle diffusion Kid C R2

2.3065 18.829 0.8803

1.9628 6.395 0.9592

0.8448 6.459 0.9304

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Fig. 7. Kinetic modelling of the adsorption of Pb(II) on MCGO composite material, (a) pseudo first order kinetic plot, (b) pseudo second order kinetic plot, (c) intra-particle diffusion plot.

experimental data from the Pb(II) adsorption on to MCGO composite adsorbent material is in good agreement with Langmuir isotherm model. This reveals that the MCGO composite adsorbents containing the homogeneous functional sites are distributed uniformly on their surface. Hence, the adsorption of Pb(II) follows the mono-layer adsorption process. The chelation adsorption process for Pb(II) gives the controlled monolayer adsorption. 3.3. Desorption and regeneration The MCGO composite adsorbent material was evaluated for regeneration and reusability. Adsorption-desorption experiments were carried

out with an initial concentration of 50 mg/L under optimal conditions for four consecutive cycles. The adsorbent material was collected using external magnet after each cycle from the solution and dried in an oven for 65 °C for 2 h. The residual concentrations of Pb(II) was analysed. Later, desorption experiments were carried out using 1 g/L of MCGO composite loaded with Pb(II) in 10 mL of 0.1 M HCl solution. Desorption study was performed at 120 rpm at 27 °C for 3 h. The results depicts, adsorption percentage of Pb(II) by MCGO composite material decreased from 92% to 78% after four consecutive cycles. Thus MCGO composite material can be recycled and reused for a maximum of four cycles. In order to investigate the practical application ability of the MCGO composite material, the real wastewater was used. The leather

Fig. 8. (a) Langmuir isotherm plot, (b) Freundlich isotherm plot for removal of Pb(II) using MCGO composite material.

M.S. Samuel et al. / International Journal of Biological Macromolecules 115 (2018) 1142–1150 Table 2 Equilibrium isotherm parameters for the adsorption of Pb(II) by MCGO composite material based on adsorbent dosage. Isotherm models

Parameters

0.25

0.5

1.0

2.0

Langmiur

qmax (mg/g) KL (L/mg) R2 Kf (mg/g) N R2

112.35 0.076 0.9624 17.344 2.906 0.9512

76.92 0.0902 0.9822 3.314 2.63 0.9569

80.64 0.255 0.9928 9.157 2.45 0.9753

41.15 0.289 0.9938 0.7676 2.481 0.9799

Freundlich

industry wastewater from Vellore, Tamil Nadu was taken for inspection. In which suspended white floccule and solid particles were found at pH at 2.50. In addition, we added Pb(NO3)2 in to the real wastewater until the concentration of Pb(II) reaches 50 mg/L due to less concentration of Pb(II) ions. The MCGO composite material shows only 80% adsorption capacity for real wastewater. The decrease in adsorption percentage may due to the practical wastewater, which contains organic matters, salts, etc. All these have slight effect on the adsorption capacity of MCGO composite material. Therefore, this material can be economically effective in adsorbing Pb(II) ions from industrial waste water. 3.4. Cell morphology and toxicity studies The MCGO composite materials was incubated along with the cells, the cell morphology changes slightly and were noted to assess the outcome of MCGO composite material on A549 cells (Fig. S5†). At lower concentration (50 μg) there is no significant difference among the MCGO composite material treated cells, the control cells showed higher growth in comparison to the MCGO composite material treated cells. Whereas increase in MCGO composite material concentrations upon 150 and 200 μg there occurs a noteworthy modification in the cell morphology in assessment to the control cells. The outcome from our study demonstrates MCGO composite material at lower concentration exposed a good biocompatibility to A549 cells. The toxicity of MCGO composite material towards A549 cells was assessed. The A549 cells were cultured in the presence of various concentrations ranging from 50 to 250 μg and the toxicity was measured after 24 h of incubation. The viable cells in cultures with MCGO composite material show about 53.7% at 50 μg and 44.8% at 100 μg concentrations. When the concentrations of MCGO composite material was increased N100 μg, the viable cell percentage decreased drastically and showed only 32.97% at 150 μg and 25.47% at 200 μg (Fig. S6†). In a study, iron oxide nanoparticles were coated on different sized graphene oxide ranging 0.5 to 7.0 μm was prepared and in vitro study was evaluated. Here, the GO-Fe3O4 and GO samples showed best biocompatibility at concentration 12.5 μg/mL. The highest reduction of cell viability occurred at a dose of 100 μg/mL in GO. Chang et al. 2011, in his study proved the preparation method of GO has influence on cell viability. Here cell viability was carried out using CCK-8 assay and A549 cells [27]. Chang et al. 2011, in his study, prepared GO samples with varying size (s-GO smaller size, l-GO larger size, and m-GO medium size) was treated on cells and found mGO effect on cell cultures was insignificant at the concentration range of 100 to 200 μg/mL. It was noted the cell viability decreased when s-GO treated at concentration between 50 and 200 μg/mL. When Fe3O4 MgNPs with 100 μg/mL was tested on A549 cell line for 72 h causes substantial reduction of cell viability [28]. In our study Fe3O4 nanoparticle above 150 μg showed reduced cell viability. Whereas Fe3O4 nanoparticle below 150 μg does not show significant change in the cell viability. The main reason to assess the MCGO composite material in vitro study was to explore the nanomaterial properties in environmental system and interface with the living stock. The major physical parameters such as particle size, shape and surface coating can induce a toxic reaction by aggregation and coagulation. In this study, we have clearly demonstrated the response of cells towards individual materials and in combination.

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Table 3 Comparison of adsorption capacities of various adsorbents for Pb(II). S. No.

Adsorbent material

qmax (mg/g)

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Iron oxide magnetic nanoparticles Fe3O4@C magnetic composites Magnetic chitosan/graphene oxide Fe3O4@Chitosan Fe3O4-NH2 Fe3O4@SiO2-SH GO-chitosan-poly(acrylic acid) Graphene oxide magnetic nano-sorbent MCGO composite material

76.9 71.42 76.94 31.6 369 91.5 138.89 73.52 112.35

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Hence, these materials can be suitable material for environmental cleanup process and biomedical application. 3.5. Performance evaluation A assessment among adsorption capacities of the synthesized MCGO composite material and other adsorbents for the removal of Pb(II) in the literature are listed in Table 3. The differences in the adsorption capacities might be due to structural morphology, surface area and functional groups of the adsorbent. It was found that MCGO composite material showed maximum adsorption capacity (112.35 mg/g) and it is been compared with some of the earlier reported materials. Hence, it can be used as a promising adsorbent in the removal of Pb(II) ions. 4. Conclusion The MCGO composite material has shown a high potential and adsorption capacity for the removal of Pb(II) ions from aqueous solutions. It was estimated that with an initial concentration of 50 mg/L, 92% of Pb (II) ions were removed at an equilibrium time of 420 min, a pH of 5, adsorbent dosage of 1 g/L and at 27 °C. The thermodynamic study also reveals that the adsorption efficiency is more favourable at higher temperature. When compared to Freundlich isotherm model, Langmuir model gives a best fit for the adsorption process. Further, the obtained experimental data were fitted to pseudo-second-order kinetic model, indicating the adsorption of Pb(II) ions onto MCGO composite material is through chemisorption process. We have also examined the biocompatibility of Fe3O4, GO and MCGO composite material nanoparticles on A549 cell line. Finally, this MCGO composite material can be applied for reusable and competent adsorbent in Pb(II) removal from industrial waste water. Acknowledgement Dr. Melvin Samuel. S is deeply thankful to Indian Institute of Technology Kharagpur for the fellowship. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.ijbiomac.2018.04.185. References [1] M. Machida, T. Mochimaru, H. Tatsumoto, Lead(II) adsorption onto the graphene layer of carbonaceous materials in aqueous solution, Carbon N. Y. 44 (2006) 2681–2688. [2] Y.H. Li, Z. Di, J. Ding, D. Wu, Z. Luan, Y. Zhu, Adsorption thermodynamic, kinetic and desorption studies of Pb2+ on carbon nanotubes, Water Res. 39 (2005) 605–609. [3] P.B. Tchounwou, C.G. Yedjou, A.K. Patlolla, D.J. Sutton, Heavy Metals Toxicity and the Environment PaulBasel 2010. [4] L. Järup, Hazards of heavy metal contamination, Br. Med. Bull. 68 (2003) 167–182. [5] K. Li, Z. Zheng, Y. Li, Characterization and lead adsorption properties of activated carbons prepared from cotton stalk by one-step H3PO4 activation, J. Hazard. Mater. 181 (2010) 440–447.

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