Competitive adsorption of heavy metal ions on carbon nanotubes and the desorption in simulated biofluids

Journal of Colloid and Interface Science 448 (2015) 347–355

Contents lists available at ScienceDirect

Journal of Colloid and Interface Science www.elsevier.com/locate/jcis

Competitive adsorption of heavy metal ions on carbon nanotubes and the desorption in simulated biofluids Xin Ma a,1, Sheng-Tao Yang b,1, Huan Tang c, Yuanfang Liu a,c, Haifang Wang a,⇑ a

Institute of Nanochemistry and Nanobiology, Shanghai University, Shanghai 200444, China College of Chemistry and Environment Protection Engineering, Southwest University for Nationalities, Chengdu 610041, China c Beijing National Laboratory for Molecular Sciences, College of Chemistry and Molecular Engineering, Peking University, Beijing 100871, China b

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

a r t i c l e

i n f o

Article history: Received 24 January 2015 Accepted 13 February 2015 Available online 23 February 2015 Keywords: Carbon nanotubes Adsorption Desorption Biofluid Toxicity Synergistic effect

a b s t r a c t Carbon nanotubes (CNTs) had meaningful adsorption capacities for Pb2+, Cu2+, Zn2+ and Cd2+, while Pb2+ showed the highest adsorption in the competitive adsorption evaluations. The desorption behaviors of heavy metal ions were completely different in various biofluids, where the desorption was significantly influenced by pH and the presence of proteins/other cations. The desorption was most effective in simulated stomach juice, and much less effective in other simulated biofluids. More Pb2+ stuck to CNTs than others, resulting in less desorption. Interestingly, the competitive desorption behaviors of four ions were largely changed comparing to the individual desorption behaviors. The implications to the biosafety evaluations and synergistic effects of CNT are discussed. Ó 2015 Elsevier Inc. All rights reserved.

1. Introduction Carbon nanomaterials have attracted great interests for their unique structure and fascinating properties [1,2]. In particular, sp2 carbon nanomaterials, such as carbon nanotubes (CNTs), fullerene and graphene, have lots of attractive applications in many important fields, including energy [3], electronics [4], material ⇑ Corresponding author. Fax: +86 21 66135275. 1

E-mail address: [email protected] (H. Wang). The authors contributed equally.

http://dx.doi.org/10.1016/j.jcis.2015.02.042 0021-9797/Ó 2015 Elsevier Inc. All rights reserved.

[5], biomedical area [6] and environment [7,8]. For instance, CNTs have been used for drug delivery [9], bioimaging [10], biodefense [11], photothermal treatment [12]. The applications of CNTs as adsorbents in water treatment have also been widely investigated, showing very high adsorption capacity for various pollutants [13–16]. Due to the valuable applications and great potential, the biosafety of carbon nanomaterials has been widely concerned [17–19]. Recently, the synergistic toxicity of CNTs and heavy metals has aroused great interest [20–22]. Several studies showed that CNTs could worsen the toxicity of heavy metal ions. Kim et al. reported

348

X. Ma et al. / Journal of Colloid and Interface Science 448 (2015) 347–355

that CNTs could interact strongly with normal organic matter to release the binding Cu2+, which induced toxicity to Daphniamagna [23]. They also found that CNTs enhanced the toxicity of Cu2+ to Daphniamagna by improving the bioavailability of Cu2+ [24]. Martinez et al. reported that CNTs enhanced the toxicity of Pb2+ to freshwater fish [25]. It was speculated that the adsorption of Pb2+ on CNTs was related to the enhanced toxicity. Qin et al. reported that CNTs enhanced the toxicity of Pb2+ to Daphniamagna, in particular at higher pH values [26]. However, the available studies mainly focused on describing the synergistic effects rather than the underneath mechanism. To fully understand the underneath mechanism, the first step is to investigate the competitive adsorption and desorption of heavy metals on CNTs in biological systems. Herein, we systematically evaluated the adsorption/desorption behaviors of heavy metal ions on oxidized CNTs in simulated biofluids. The adsorption isotherms and kinetics of Pb2+, Cu2+, Zn2+ and Cd2+ on CNTs were measured. The competitive adsorption of the four ions on CNTs was evaluated. The desorption behaviors of Pb2+, Cu2+, Zn2+ and Cd2+ from CNTs in simulated biofluids were investigated one-by-one and also in a competitive way. Our results clearly showed that CNTs adsorbed heavy metal ions fast and effectively. The desorption of heavy metal ions from CNTs was influenced by pH and the presence of proteins/cations in biofluids. Pb2+ showed higher affinity to CNTs and lower desorption. The competitive desorption of four ions showed quite different behaviors from individual desorption. The implications to the biosafety evaluations and synergistic effects of CNT are discussed. 2. Materials and methods 2.1. Materials MWCNTs with outer diameters of 10–20 nm and lengths of 5– 15 lm were purchased from Shenzhen Nanotechnologies Port Co. Ltd., China. Uric acid, glucosaminhydrochloride, mucin (from porcine stomach), pepsin (from porcine gastric mucosa), pancreatin (from porcine pancreas), lipase (from porcine pancreas) were obtained from Sigma, and glucuronic acid was obtained from Alfa Aesar. Dlbecco’s modified eagle medium (DMEM) were purchased from Hangzhou Gino Biological Pharmaceutical Engineering Co. Ltd., China. Bovine serum albumin (BSA) was obtained from Dingguo Biotechnology Co. Ltd., China. Bovine serum was bought from Sijiqing Biological Engineering Co. Ltd., China. All other chemicals were of analytical grade and supplied by Sinopharm Chemical Reagent Co. Ltd., China. The simulated gastric juice and intestinal juice were prepared following the recipes listed in Table 1, which was given by Peters et al. [27]. 2.2. Oxidation of MWCNTs MWCNTs (1.0 g) were dispersed in 400 mL of concentrated H2SO4/HNO3 mixture (V:V = 3:1) and sonicated for 6 h. After cooling to room temperature, MWCNTs were washed with deionized water to near neutral. MWCNTs were then centrifuged at 20,000g for 15 min and the sediment was dried at 70 °C for 24 h to obtain

Fig. 1. Representative TEM image (a) and IR spectrum (b) of O-MWCNTs.

the O-MWCNTs. O-MWCNTs were characterized with infrared (IR) spectrometer (Avatar 370, Thermo Nicolet, USA) and transmission electron microscopy (TEM, JEM-200CX, Hitachi, Japan). 2.3. Adsorption behaviors We firstly investigated the adsorption behaviors of Pb2+, Cu2+, Zn2+ and Cd2+ on O-MWCNTs individually. In the kinetics study, 5 mg of O-MWCNTs were added to 6 mL of heavy metal solution separately (Pb2+: 140 mg/L; Cu2+: 40 mg/L; Zn2+: 40 mg/L; Cd2+: 40 mg/L; pH = 5). The mixture was shaken at 25 °C and collected for metal concentration determination at different time intervals. The mixtures were centrifuged at 30,000g for 10 min before the inductive coupling plasma-atomic emission spectrometer (ICP-AES, Prodigy, Leeman Labs, USA) measurement. The kinetics data of heavy metals were fitted to pseudo-second-order model (Eq. (1)). In the isothermal adsorption study, 5 mg O-MWCNTs were added to 6 mL of heavy metal solution (Pb2+: 0–200 mg/L; Cu2+: 0–60 mg/L; Zn2+: 0–80 mg/L; Cd2+: 0–60 mg/L; pH = 5). The mixture was shaken at 25 °C for 2 h and collected for metal

Table 1 Recipes of simulated gastric and intestinal juice for 1 L.

Gastric juice (pH 1.3 ± 0.1) Intestinal juice (pH 8.1 ± 0.1)

Inorganic constituents

Organic constituents

2752 mg NaCl, 824 mg KCl, 306 mg NaH2PO4H2O, 302 mg CaCl2, 650 mg glucose, 20 mg glucuronic acid 7012 mg NaCl, 80 mg KH2PO4, 564 mg KCl, 50 mg MgCl26H2O, 151 mg CaCl2, 3388 mg NaHCO3, 180 lL HCl (37%)

85 mg urea, 3 g mucin, 330 mg glucosaminhydrochloride, 1 g BSA, 2.5 g pepsin 100 mg urea,1 g BSA, 1.5 g lipase, 4.5 g pancreatin

X. Ma et al. / Journal of Colloid and Interface Science 448 (2015) 347–355

349

Fig. 2. Adsorption isotherms of heavy metal ions on O-MWCNTs. Data are presented as mean ± SD (n = 3).

Table 2 Parameters of the Langmuir model for the adsorption of heavy metal ions on OMWCNTs.

qm b R

Pb2+

Cu2+

Zn2+

Cd2+

76.7 0.280 0.988

15.3 3.13 0.988

13.6 0.545 0.987

32.2 0.380 0.994

concentration determination. The mixtures were centrifuged at 30,000g for 10 min and the supernatants were measured by ICP-AES. The maximum adsorption capacity was calculated following the Langmuir model (Eq. (2)).

t 1 t ¼ þ qt k2 q2e qe 1 1 1 ¼ þ qe qm bqm C e

ð1Þ ð2Þ

Then, the adsorption behaviors were investigated in the competitive way. In the kinetics study, 5 mg of O-MWCNTs were added to 6 mL of heavy metal mixture solution. Pb2+, Cu2+, Zn2+ and Cd2+ were of the same concentrations of 60 mg/L. The mixture was shaken at 25 °C and collected for metal concentration determination at different time intervals. The mixtures were centrifuged at 30,000g for 10 min and the supernatants were measured by ICP-AES. In the isothermal adsorption study, 5 mg O-MWCNTs were added to 6 mL of heavy metal mixture solution. Pb2+, Cu2+, Zn2+ and Cd2+ were of the same concentrations in the range of 0–200 mg/L. The mixture was shaken at 25 °C for 2 h and collected for metal

concentration determination. The mixtures were centrifuged at 30,000g for 10 min and the supernatants were measured by ICP-AES. 2.4. Desorption behaviors Similarly, we firstly investigated the desorption behaviors of absorbed metal ions from O-MWCNTs individually. Five mg of O-MWCNTs saturated with heavy metal ions were dispersed into 6 mL of different media, including water (pH 7.4), water (pH 1), PBS (0.01 M, pH 7.4), normal saline (pH 7.4), BSA aqueous solution (40 mg/mL, pH 7.4), BSA aqueous solution (40 mg/mL, pH 5.5), simulated gastric juice (pH 1.3), simulated intestinal juice (pH 8.1), DMEM medium (with 10% fetal bovine serum, pH 7.4) and the mixtures were shaken at 37 °C. At designed time intervals (0–24 h), the mixtures were centrifuged at 30,000g for 10 min and the supernatants were measured for the concentrations of free metal ion in solution by ICP-AES. The desorption rate was calculated from Eq. (3) (c: the ion concentration in supernatant; V: the volume of supernatant; qe: the adsorption capacity):

Desorptionð%Þ ¼

cV  100% qe

ð3Þ

Then, we investigated the desorption behaviors of absorbed metal ions from O-MWCNTs in a competitive way. Two gram of O-MWCNTs were saturated with heavy metal mixture solution (Pb2+, Cu2+, Zn2+ and Cd2+ were of the same concentrations of 2000 mg/L) and collected for the desorption study. Five mg of O-MWCNTs with heavy metal ions were dispersed into 6 mL of

350

X. Ma et al. / Journal of Colloid and Interface Science 448 (2015) 347–355

Fig. 3. Adsorption kinetics of heavy metal ions on O-MWCNTs. Data are presented as mean ± SD (n = 3).

Table 3 Pseudo-second-order model analyses for the adsorption kinetics of Pb2+, Cu2+, Zn2+ and Cd2+ on O-MWCNTs. Ion 2+

Pb Cu2+ Zn2+ Cd2+

qe,exp (mg/g)

qe,cal (mg/g)

k2 (g/(mg min))

R

73.4 16.3 13.4 26.7

74.0 16.3 13.6 26.7

0.0191 0.385 0.0472 0.140

0.9999 0.9999 0.9999 0.9999

different media, including water (pH 7.4), water (pH 1), PBS (0.01 M, pH 7.4), normal saline (pH 7.4), BSA aqueous solution (40 mg/mL, pH 7.4), BSA aqueous solution (40 mg/mL, pH 5.5), simulated gastric juice (pH 1.3), simulated intestinal juice (pH 8.1), DMEM medium (pH 7.4) and the mixtures were shaken at 37 °C. At designed time intervals (0–24 h), the concentrations of free metal ion in solution were determined as described above. 3. Results and discussion 3.1. Characterization of O-MWCNTs CNTs adsorb metal ions more effectively in oxidized forms. Therefore, we oxidized MWCNTs with H2SO4/HNO3 into O-MWCNTs following our previous reports [28,29]. O-MWCNTs were shortened to 200–800 nm in length (Fig. 1a). Carboxyl groups and hydroxyl groups were evidenced by the strong absorption at 3440 cm1 in the IR spectrum (Fig. 1b). The C@O bonds were indicated by the peak at 1700 cm1. The CAO bonds were confirmed by the peak at 1100 cm1. As reported in the literature, other oxygen

forms, including carbonyl groups, epoxy groups and hydroxyl groups, might also be introduced during the oxidation process [28]. The f-potential of O-MWCNTs at pH 7 was 42.2 mV, which should be attributed to the oxygen containing groups. Negative charges of O-MWCNTs benefited the adsorption of metal ions because of the strong electrostatic interaction. 3.2. Adsorption behaviors The adsorption of heavy metal ions on CNTs has been widely reported [30]. Our results are well consistent with the results in the literature [31–35]. As shown in Fig. 2, O-MWCNTs adsorb Pb2+, Cu2+, Zn2+ and Cd2+ effectively. With the increase of metal concentrations, the adsorption capacity increases quickly at low concentrations. At high concentrations, the adsorption capacity gradually reaches the maximum, indicating the full occupation of absorptive sites on O-MWCNTs. All four ions follow similar trend, where Pb2+ shows the highest adsorption capacity. This is consistent with the results obtained by Li et al. [34]. The high adsorption capacity of Pb2+ indicated that more sites on O-MWCNTs were available for Pb2+. According to the b values of Langmuir model (Table 2), the binding strength between Pb2+ and O-MWCNTs is the weakest and the binding strength between Cu2+ and O-MWCNTs is the strongest. This should be due to that Pb2+ occupies more binding sites and the average binding strength is weak. Cu2+ only binds to those of high affinity, thus has the strongest binding strength. Reflecting in the adsorption isotherms, the curve of Cu2+ increased very sharply in the initial stage and reached the equilibrium within 10 min. The maximum adsorption capacities of O-MWCNTs for metal ions are also listed in Table 2.

X. Ma et al. / Journal of Colloid and Interface Science 448 (2015) 347–355

The adsorption kinetics of heavy metal ions on O-MWCNTs was generally fast (Fig. 3). The adsorption reaches equilibrium within 30 min for all four ions. The oxidation enabled the good dispersion of O-MWCNTs in solution, thus the diffusion of ions toward O-MWCNTs was easy, which consequently resulted in the fast adsorption kinetics [33]. The adsorption kinetics of Pb2+, Cu2+, Zn2+ and Cd2+ could be described well by the pseudo-second-order model (Table 3). According to the fitting parameters, the adsorption of Cu2+ was the fastest one and the adsorption of Pb2+ was slowest. It is difficult to distinguish them in Fig. 3 because of the quick adsorption kinetics. The calculated adsorption capacity (qe,cal) is very close to the experimental one (qe,exp), indicating the success of fitting. When the adsorption is performed in the competitive way, the fast adsorption kinetics retains (Fig. 4). However, the adsorption capacity for each ion decreases. The adsorption rate decreases 41.6% for Pb2+, 15.6% for Cu2+, 81.5% for Zn2+ and 89.7% for Cd2+. This indicated that the competition led to the decrease of the adsorption capacity of all ions. Similar to the individual adsorption, Pb2+ shows the highest adsorption capacity. Cu2+ had the strongest binding affinity according to the largest b value, thus the decrease of its adsorption capacity was minimum. Zn2+ and Cd2+ had the largest decrease in adsorption capacity, implying the low binding affinity. The results here suggested that CNTs would bind to Pb2+ and Cu2+ more when entering polluted water. The competitive adsorption behaviors were consistent with the results in literature [34]. The adsorption of heavy metal ions on CNTs might have important implication to the synergistic toxicity of CNTs and heavy metals. Many papers documented that CNTs could be used as delivery vehicles for drugs to improve the bioavailability of drugs [36,37]. Kim et al. reported that CNTs improved the bioavailability of Cu2+ to Daphniamagna, which resulted in higher heavy metal toxicity [24]. Martinez et al. attributed the enhanced toxicity of Pb2+in the presence of CNTs to the adsorption of Pb2+ on CNTs [25]. Qin et al. suggested that Daphniamagna might take CNTs as food, where Pb2+ adsorbed on CNTs could enter the body to induce toxicity [26]. Similar phenomena were observed in the synergistic toxicity of CNTs and other pollutants. Hu et al. found that sodium pentachlorophenate adsorbed on CNTs and synergistic toxicity presented [38]. The synergistic toxicity of 4-nonylphenol [39] and diuron [40] with CNTs was also reported. Beyond CNTs, the synergistic toxicity of other nanomaterials and pollutants were found, again indicating the importance of such investigations [41,42]. Our results clearly indicated that heavy metal ions adsorbed on CNTs fast with meaningful capacity. Once CNTs enter the environment, the adsorption occurs immediately and the toxicity of heavy metal ions would be enhanced. Thus, the discharge of CNTs into environment should be strictly limited, although the toxicity of CNTs alone is not so serious [43,44].

351

and BSA (both pH 7.4 and 5.5), and the desorption rates are low in water (pH 7.4), saline (pH 7.4), PBS (pH 7.4) and simulated intestinal juice (pH 8.1). Zn2+ and Cd2+ desorbs much more than Pb2+ and Cu2+. The desorption rates of Zn2+ and Cd2+ are only low in PBS (pH 7.4) and water (pH 7.4). Interestingly, lower pH in aqueous fluids benefits the desorption, but in the presence of proteins higher pH seems better. The desorption rates of all ions are higher in BSA solution (pH 7.4) than those in BSA solution (pH 5.5). Another issue should be noticed was that heavy metal ions desorbed more in saline than in PBS, where both saline and PBS were inorganic salts. The competitive desorption was performed in aforementioned biofluids, too. The desorption behaviors show significant changes for all four ions (Table 4 and Fig. 6). In the simulated gastric juice, the desorption rates are very high for all four ions, similar to the individual desorption evaluations. In simulated intestinal juice, the desorption of Pb2+ is slightly enhanced and the desorption of Cu2+ is promoted from 13.6% in individual desorption to 95.6% in competitive desorption. In contrast, the desorption of Zn2+ and Cd2+ was seriously inhibited in competitive desorption (23.4% for Zn2+ and 20.2% for Cd2+), comparing to the individual desorption (71.6% for Zn2+ and 57.9% for Cd2+). In DMEM (pH 7.4), the desorption of Pb2+ is not affected, and Cu2+ completely desorbs from O-MWCNTs. The desorption of Zn2+ and Cd2+ is inhibited again. In saline, the desorption of Pb2+ and Cu2+ is moderately inhibited, while the desorption of Zn2+ and Cd2+ is promoted. In PBS, the

3.3. Desorption behaviors The desorption studies reported before usually focused on the repeated availability performance of metal ions sorption onto CNTs for reducing the cost [45]. The regeneration solution with lower pH is used. However, there is no study on the desorption of metal ions from CNTs in biosystems. The desorption of heavy metal ions from O-MWCNTs in simulated biofluids was firstly investigated individually. As shown in Fig. 5, completely different desorption behaviors of heavy metal ions are recorded in different biofluids. All ions show high desorption rate in water (pH 1) and simulated gastric juice (pH 1.3), which is well consistent with the published data [45]. Pb2+ has the lowest desorption rates in other biofluids (Table 4). The Pb2+ concentrations in simulated intestinal juice are even lower than the detection limit of ICP-AES (0.00001 mg/mL). Cu2+ desorbs more in DMEM (pH 7.4)

Fig. 4. Competitive adsorption behaviors of heavy metal ions on O-MWNTs. (a) adsorption isotherms; (b) adsorption kinetics. Data are presented as mean ± SD (n = 3).

352

X. Ma et al. / Journal of Colloid and Interface Science 448 (2015) 347–355

Fig. 5. Desorption behaviors of heavy metal ions from O-MWCNTs in different aqueous fluids. Data are presented as mean ± SD (n = 3).

Table 4 Desorption rates of heavy metal ions in individual and competitive evaluations after 24 h incubation. Pb2+

Gastric juice Intestinal juice DMEM (pH 7.4) Saline PBS (pH 7.4) BSA (pH 5.5) BSA (pH 7.4) Water (pH 1) Water (pH 7.4)

Cu2+

Zn2+

Cd2+

Individual (%)

Competitive (%)

Individual (%)

Competitive (%)

Individual (%)

Competitive (%)

Individual (%)

Competitive (%)

100 0 0.05 11.3 7.2 27.6 28.4 93.3 3.5

99.5 0.35 0.16 3.8 0.007 17.1 19.8 95.8 0.13

98.2 13.6 83.6 20.2 0.73 81.6 91.8 91.0 5.5

96.7 95.6 100 9.2 0.81 73.7 72.0 99.3 8.3

99.7 71.6 80.9 51.8 3.2 80.5 92.0 99.3 5.5

97.0 23.4 61.2 88.1 10.7 90.0 55.2 98.0 61.2

98.6 57.9 69.5 58.5 13.7 66.0 99.8 97.1 3.4

88.5 20.2 48.2 88.0 0.32 52.2 54.2 92.5 53.2

desorption of Pb2+ and Cd2+ is inhibited and the desorption of Cu2+ and Zn2+ is enhanced. Although it is very hard to tell the guidelines for the competitive desorption, apparently pH retains its significant influence on the competitive desorption. In acidic gastric juice, O-MWCNTs had the dominating desorption of heavy metal ions. As shown in Fig. 7, at pH 1, near complete desorption is observed for all ions. In acidic water, there was no other additive except for HCl. This suggested that the low pH was the main reason for the high desorption rate. In acidic BSA, higher desorption of Zn2+ is shown, while that of the rest metal ions are similar, indicating the importance of protein. Comparing to neutral water, BSA promotes the desorption of Pb2+ and Cu2+ and slightly inhibits that of Zn2+. These phenomena suggested that proteins affects the competitive desorption and the effects are regulated by pH.

The mechanism of the pH regulated desorption might be explained by the f-potential of O-MWCNTs at different pH values. As shown in Fig. 8, at acidic pH 1, the f-potential was 13.2 mV, much higher than that at pH 7 (42.2 mV). This suggested at acidic pH the negative charges of O-MWCNTs reduced. The less charge led to the weaker electrostatic interaction between O-MWCNTs and metal ions, which consequently enhanced the desorption of metal ions from O-MWCNTs. In the contrast, ionic strength had less influence on the desorption of heavy metal ions from O-MWCNTs (data not shown). The desorption of heavy metal ions from CNTs has been widely reported in the adsorbent developments by using diverse eluents, but not biosystems [46]. When metal-CNTs enter biosystems, the biomolecules/inorganic components might bind to CNTs [47,48] and the chelation of heavy metal ions with biomolecules might

X. Ma et al. / Journal of Colloid and Interface Science 448 (2015) 347–355

353

Fig. 6. Competitive desorption behaviors of heavy metal ions from O-MWCNTs in different simulated biofluids (a) simulated gastric juice; (b) simulated intestinal juice; (c) DMEM; (d) saline and (e) PBS at pH 7.4.

occurs, too [49]. These will lead to the release of heavy metal ions to biosystems and consequently induce toxicity. Our results clearly showed that such release of heavy metals to biosystems was possible. The two important factors pH and proteins affecting the desorption are easily available in biosystems. Therefore, in the toxicity studies on CNTs, the release of metal ions should be carefully considered. For example, CNTs might act as vehicles that shuttle heavy metal ions into cells and release the ions intracellular. The release of metal impurities from CNTs has been regarded as one of the toxicological mechanism of CNTs [50]. Thus, the delivery of heavy metal by CNTs might induce serious

toxicity. Therefore, to monitor the delivery and release of heavy metal ions at cellular level is worthwhile. Another issue should be investigated is the bioavailability of heavy metals in the presence of CNTs, because CNTs are hardly absorbed in gastrointestinal tract [18,43], but the binding/release of heavy metals would occur in gastrointestinal tract. The released heavy metal ions might across the intestine, enter the blood circulation and inducing the adverse health effect [51,52]. Moreover, considering that CNTs are frequently used in heavy metal adsorption in water treatment [53], the discharge of used CNT adsorbents should be strictly avoided.

354

X. Ma et al. / Journal of Colloid and Interface Science 448 (2015) 347–355

Fig. 7. Competitive desorption behaviors of heavy metal ions from O-MWCNTs in different environment. (a) BSA at pH 5.5; (b) BSA at pH 7.4; (c) water at pH 1 and (d) water at pH 7.4.

water/PBS and basic simulated intestinal juice. Pb2+ stuck to CNTs tightly with less desorption. We hope that our results will benefit the ongoing synergistic toxicity evaluations of carbon nanomaterials. Acknowledgments We acknowledge financial support from the China Ministry of Science and Technology (973 Project No. 2011CB933402), the China Natural Science Foundation (No. 201307101), and the Science and Technology Department of Sichuan Province (Pillar Program No. 20134FZ0060). References

Fig. 8. f-potential of O-MWCNTs at different pH values.

4. Conclusions In summary, the competitive adsorption of heavy metal ions on O-MWCNTs and the desorption in biofluids have been investigated. O-MWCNTs had meaningful adsorption capacities for Pb2+, Cu2+, Zn2+ and Cd2+, where Pb2+ showed the highest adsorption in both individual and competitive evaluations. After entering biofluids, the heavy metal ions desorbed from O-MWCNTs, in particular under acidic conditions. The desorption was most effective in simulated stomach juice, and much less effective in neutral

[1] S. Beg, M. Rizwan, A.M. Sheikh, M.S. Hasnain, K. Anwer, K. Kohli, J. Pharm. Pharmacol. 63 (2011) 141. [2] B.K. Gorityala, J. Ma, X. Wang, P. Chen, X.W. Liu, Chem. Soc. Rev. 39 (2010) 2925. [3] M.F. De Volder, S.H. Tawfick, R.H. Baughman, A.J. Hart, Science 339 (2013) 535. [4] H. Tamura, R. Martinazzo, M. Ruckenbauer, I. Burghardt, J. Chem. Phys. 137 (2012) 22A540. [5] A. Cao, Z. Liu, S. Chu, M. Wu, Z. Ye, Z. Cai, Y. Chang, S. Wang, Q. Gong, Y. Liu, Adv. Mater. 22 (2010) 103. [6] Z. Liu, S. Tabakman, K. Welsher, H. Dai, Nano Res. 2 (2009) 85. [7] S.T. Yang, J.B. Luo, J.H. Liu, Q.H. Zhou, J. Wan, C. Ma, R. Liao, H.F. Wang, Y.F. Liu, Nanosci. Nanotechnol. Lett. 5 (2013) 372. [8] S.T. Yang, S. Chen, Y. Chang, A. Cao, Y. Liu, H. Wang, J. Colloid Interface Sci. 359 (2011) 24. [9] Z. Yang, Y. Zhang, Y. Yang, L. Sun, D. Han, H. Li, C. Wang, Nanomedicine 6 (2010) 427. [10] A. De la Zerda, C. Zavaleta, S. Keren, S. Vaithilingam, S. Bodapati, Z. Liu, J. Levi, B.R. Smith, T.J. Ma, O. Oralkan, Z. Cheng, X. Chen, H. Dai, B.T. Khuri-Yakub, S.S. Gambhir, Nat. Nanotechnol. 3 (2008) 557.

X. Ma et al. / Journal of Colloid and Interface Science 448 (2015) 347–355 [11] H. Wang, L. Gu, Y. Lin, F. Lu, M.J. Meziani, P.G. Luo, W. Wang, L. Cao, Y.P. Sun, J. Am. Chem. Soc. 128 (2006) 13364. [12] H.K. Moon, S.H. Lee, H.C. Choi, ACS Nano 3 (2009) 3707. [13] G. Andrade-Espinosa, E. Munoz-Sandoval, M. Terrones, M. Endo, H. Terrones, J.R. Rangel-Mendez, J. Chem. Technol. Biotechnol. 84 (2009) 519. [14] X.Y. Yu, T. Luo, Y.X. Zhang, Y. Jia, B.J. Zhu, X.C. Fu, J.H. Liu, X.J. Huang, ACS Appl. Mater. Interfaces 3 (2011) 2585. [15] H.H. Cho, K. Wepasnick, B.A. Smith, F.K. Bangash, D.H. Fairbrother, W.P. Ball, Langmuir 26 (2010) 967. [16] C.Y. Kuo, Desalination 249 (2009) 781. [17] J.H. Liu, S.T. Yang, X.X. Chen, H. Wang, Curr. Drug Metab. 13 (2012) 1046. [18] S.-T. Yang, J. Luo, Q. Zhou, H. Wang, Theranostics 2 (2012) 271. [19] H. Wang, S.T. Yang, A. Cao, Y. Liu, Acc. Chem. Res. 46 (2013) 750. [20] Q. Wei, B. Juanjuan, T. Longlong, L. Zhan, L. Peng, W. Wangsuo, Biomed. Res. Int. 2014 (2014) 463161. [21] Z.G. Yu, W.X. Wang, Water Res. 47 (2013) 4179. [22] H. Oloumi, E.A. Mousavi, R. Mohammadinejad, Agrochimica 58 (2014) 91. [23] K.T. Kim, A.J. Edgington, S.J. Klaine, J.W. Cho, S.D. Kim, Environ. Sci. Technol. 43 (2009) 8979. [24] K.T. Kim, S.J. Klaine, S. Lin, P.C. Ke, S.D. Kim, Environ. Toxicol. Chem. 29 (2010) 122. [25] D.S.T. Martinez, O.L. Alves, E. Barbieri, J. Phys: Conf. Ser. 429 (2013) 012043. [26] L. Qin, Q. Huang, Z. Wei, L. Wang, Z. Wang, Environ. Toxicol. Pharmacol. 38 (2014) 199. [27] R. Peters, E. Kramer, A.G. Oomen, Z.E. Rivera, G. Oegema, P.C. Tromp, R. Fokkink, A. Rietveld, H.J. Marvin, S. Weigel, A.A. Peijnenburg, H. Bouwmeester, ACS Nano 6 (2012) 2441. [28] S.T. Yang, H. Wang, Y. Wang, Y. Wang, H. Nie, Y. Liu, Chemosphere 82 (2011) 621. [29] Y.X. Wang, S.T. Yang, Y.L. Wang, Y.F. Liu, H.F. Wang, Colloid Surf. B: Biointerfaces 97 (2012) 62. [30] R. Kumar, M.A. Khan, N. Haq, Crit. Rev. Environ. Sci. Technol. 44 (2014) 1000. [31] F. Yu, Y. Wu, J. Ma, C. Zhang, J. Environ. Sci. 25 (2013) 195. [32] C.L. Chen, X.K. Wang, Ind. Eng. Chem. Res. 45 (2006) 9144. [33] C.Y. Lu, H.S. Chiu, Chem. Eng. Sci. 61 (2006) 1138.

355

[34] Y.H. Li, J. Ding, Z.K. Luan, Z.C. Di, Y.F. Zhu, C.L. Xu, D.H. Wu, B.Q. Wei, Carbon 41 (2003) 2787. [35] R.Y. Abuduwayiti, C. Qu, T. Yu, B. Yang, Appl. Mech. Mater. 295–298 (2013) 1227. [36] A. Bianco, K. Kostarelos, M. Prato, Curr. Opin. Chem. Biol. 9 (2005) 674. [37] Z. Liu, K. Chen, C. Davis, S. Sherlock, Q. Cao, X. Chen, H. Dai, Cancer Res. 68 (2008) 6652. [38] C.W. Hu, L.J. Zhang, W.L. Wang, Y.B. Cui, M. Li, Soil Biol. Biochem. 70 (2014) 123. [39] E. Caballero-Diaz, R. Guzman-Ruiz, M.M. Malagon, B.M. Simonet, M. Valcarcel, J. Hazard. Mater. 275 (2014) 107. [40] F. Schwab, T.D. Bucheli, L. Camenzuli, A. Magrez, K. Knauer, L. Sigg, B. Nowack, Environ. Sci. Technol. 47 (2013) 7012. [41] Y. Shi, J.H. Zhang, M. Jiang, L.H. Zhu, H.Q. Tan, B. Lu, Environ. Mol. Mutagen. 51 (2010) 192. [42] D. Wang, J. Hu, D.R. Irons, J. Wang, Sci. Total Environ. 409 (2011) 1351. [43] X. Deng, G. Jia, H. Wang, H. Sun, X. Wang, S. Yang, T. Wang, Y. Liu, Carbon 45 (2007) 1419. [44] S.T. Yang, X. Wang, G. Jia, Y. Gu, T. Wang, H. Nie, C. Ge, H. Wang, Y. Liu, Toxicol. Lett. 181 (2008) 182. [45] G.P. Rao, C. Lu, F. Su, Sep. Purif. Technol. 58 (2007) 224. [46] Y.B. Pu, X.F. Yang, H. Zheng, D.S. Wang, Y. Su, J. He, Chem. Eng. J. 219 (2013) 403. [47] S.T. Yang, Y. Liu, Y.W. Wang, A. Cao, Small 9 (2013) 1635. [48] S.H. De Paoli, L.L. Diduch, T.Z. Tegegn, M. Orecna, M.B. Strader, E. Karnaukhova, J.E. Bonevich, K. Holada, J. Simak, Biomaterials 35 (2014) 6182. [49] J.H. Shin, K.M. Lim, J.Y. Noh, O.N. Bae, S.M. Chung, M.Y. Lee, J.H. Chung, Chem. Res. Toxicol. 20 (2007) 38. [50] X. Liu, V. Gurel, D. Morris, D.W. Murray, A. Zhitkovich, A.B. Kane, R.H. Hurt, Adv. Mater. 19 (2007) 2790. [51] M.B. Rabinowitz, J.D. Kopple, G.W. Wetherill, Am. J. Clin. Nutr. 33 (1980) 1784. [52] W. Zhang, B. Xiong, L. Chen, K. Lin, X. Cui, H. Bi, M. Guo, W. Wang, Environ. Toxicol. Pharmacol. 36 (2013) 51. [53] A. Stafiej, K. Pyrzynska, Sep. Purif. Technol. 58 (2007) 49.