Strong corrosion induced by carbon nanotubes to accelerate Fe biodegradation

Materials Science & Engineering C 104 (2019) 109935

Contents lists available at ScienceDirect

Materials Science & Engineering C journal homepage: www.elsevier.com/locate/msec

Strong corrosion induced by carbon nanotubes to accelerate Fe biodegradation Cijun Shuaia,b,c, Sheng Lia, Guoyong Wangb, Youwen Yangb, Shuping Pengd,e, Chengde Gaoa,

T ⁎

a

State Key Laboratory of High Performance Complex Manufacturing, College of Mechanical and Electrical Engineering, Central South University, Changsha, China Jiangxi University of Science and Technology, Ganzhou, China c Shenzhen Institute of Information Technology, Shenzhen, China d NHC Key Laboratory of Carcinogenesis and The Key Laboratory of Carcinogenesis and Cancer Invasion of the Chinese Ministry of Education, Xiangya Hospital, Central South University, Changsha, China e Cancer Research Institute, School of Basic Medical Sciences, Central South University, Changsha, China b

A R T I C LE I N FO

A B S T R A C T

Keywords: Biodegradation Composites Corrosion Biocompatibility

The slow degradation of Fe severely restricts its application in bone repair although it possesses good biocompatibility and high mechanical properties. In this study, carbon nanotubes (CNTs) were introduced to accelerate Fe biodegradation: (I) CNTs acted as cathodes to induce galvanic corrosion owing to their differences in corrosion potential; (II) The large specific surface area of CNTs increased area ratios of cathode to anode; (III) The excellent electrical conductivity of CNTs allowed significant levels of electron transfer through the cathode in galvanic corrosion. Consequently, the degradation rate of Fe/CNTs composites greatly increased by 74% with the increase of CNTs (0.3–0.9 wt%). Further addition of CNTs would lead to corrosion holes and cracks due to localized corrosion. Besides, cell culture experiments showed that MG-63 cells could normally proliferate to maintain their population, indicating good cytocompatibility of Fe/CNTs composites. The results proved that the incorporation of CNTs into Fe was an effective approach to develop Fe-based bone implants with enhanced degradation rates.

1. Introduction Biodegradable Fe-based implants have attracted a great deal of attentions in orthopedic applications owing to the sufficient mechanical properties [1–3]. Moreover, Fe is an essential element to maintain the normal functions of oxygen transport and enzymatic catalysis in the human body [4,5]. Many studies on Fe have shown that there were no or very limited toxicity on cells and no side effects on tissues/organs [4,6–8]. Additionally, in comparison with Mg, Fe can maintain structural integrity and doesn't produce hydrogen in the process of degradation [9,10]. Nevertheless, the rather slow degradation of Fe in comparison with bone healing restricts its clinical applications [11–13]. Addition of noble potential phases (Au, Pt, Pd, etc.) as cathodes to form galvanic corrosion with Fe matrix is a method for accelerating the degradation [14]. Huang et al. [15] reported that Au with standard electrode potential of +0.17 V enhanced the corrosion rate of as-sintered Fe from 0.14 to 0.23 mg·cm−2·day−1 in the immersion tests. They also added Pt (standard electrode potential of +1.21 V) into Fe matrix to accelerate the degradation and the corrosion rate of as-cast Fe

⁎

increased from 0.04 to 0.19 mg·cm−2·day−1 [16]. Čapek et al. [4] introduced Pd with standard electrode potential of +0.92 V to accelerate the degradation of Fe, finding that Pd had obvious effect on increasing the corrosion rate of Fe. It should also be noted that a large amount of these phases needed to be incorporated to achieve effective improvements in degradation rate, e.g., Au up to 10 wt% [15], which may bring about uncertainties in the biocompatibility of Fe-based implants. Carbon nanotubes (CNTs) possess a higher standard electrode potential (+0.21 V) than Fe (−0.44 V) and are expected to form galvanic corrosion owing to the differences in potential. Furthermore, CNTs are acknowledged as electrical conductive reinforcing phases owing to high specific surface area, and especially excellent electrical conductivity [17–19], which will probably further enhance galvanic corrosion in Fe. On the one hand, the high specific surface area indicates that there is more surface exposure to matrix, which may increase area ratios of cathode to anode. On the other hand, the excellent electrical conductivity means that there is low electrical resistance of cathode in galvanic corrosion and allowed significant levels of electron transfer through the cathode, thereby providing a highly accelerated corrosion

Corresponding author. E-mail address: [email protected] (C. Gao).

https://doi.org/10.1016/j.msec.2019.109935 Received 13 March 2019; Received in revised form 7 June 2019; Accepted 1 July 2019 Available online 02 July 2019 0928-4931/ © 2019 Elsevier B.V. All rights reserved.

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

Co., Tokyo, Japan) at room temperature. The grain sizes of Fe/CNTs composites were represented by the mean value. Raman spectra were recorded by focused Raman spectrometer (Invia-reflex, Renishaw, Co., UK) with an excitation laser wavelength of 514.5 nm. The spectra were recorded in the region of 800–2000 cm−1 with acquisition time of 1 min and spectral resolution of 4 cm−1 and three measurements were conducted for each group. Microstructure and surface morphologies of Fe/CNTs composites after immersion in simulated body fluid (SBF) for 28 days were investigated using Phenom scanning electron microscope (SEM, Philips XL-30FEG, Amsterdam, Netherlands) equipped with energy dispersive spectroscopy (EDS) that was applied to analyze chemical composition of immersed samples. The relative density (Rρ) of Fe/CNTs composites was calculated according to the formula [25]:

environment [20,21], strongly contributing to the increase in corrosion current density. In addition, CNTs have been widely studied for biomedical applications such as tissue engineering, drug delivery, etc., which demonstrated good biocompatibility [22–24]. In this study, CNTs were employed in an attempt to accelerate the degradation of Fe and Fe/CNTs composites were prepared via selective laser melting (SLM). As a 3D printing technique, SLM process is highly flexible and especially suitable for the quick fabrication of composites with customized geometry and complex internal features. Compared with traditional fabrication methods, SLM is known as a high-scalable, time- and cost-saving technique without the need of expensive design and processing of both molds and supporting structures. Their biodegradation behavior was investigated and the corresponding corrosion mechanism was discussed in detail. The microhardness, compression strength and bending strength of Fe/CNTs composites were measured. Besides, the cytocompatibility of the composites was evaluated by in vitro tests.

(

)

Rρ = 1 − Apore Atot × 100%

(1)

2. Materials and procedures

in which Apore was the sum areas of pores and Atot was the total examined areas, respectively.

2.1. Fabrication of the Fe/CNTs composites

2.3. Mechanical property tests

The Fe/CNTs composites and Fe were fabricated via selective laser melting of Fe and CNTs powders. As shown in Fig. 1, preparing procedures of Fe/CNTs composites were as follows. CNTs were firstly added into a beaker containing ethanol and they were ultrasonically vibrated for 2 h to obtain dispersed CNTs, as shown in Fig. 1(a). The dispersed CNTs were gradually added to another beaker containing Fe powder. Then the mixed powders were mechanically stirred at a speed of 200 rpm and vibrated using ultrasonic for 2 h at room temperature, as shown in Fig. 1(b). Subsequently, the Fe/CNTs powders were filtrated using a funnel and dried for 10 h at 50 °C to completely remove the ethanol, as illustrated in Fig. 1(c). The selective laser melting process was shown in Fig. 1(d), in which the powders were scanned and heated by laser beam, making a layer of powders completely melted. The duration of laser step on powders was approximately 0.5–25 ms. Afterwards, the melting platform moved down by a thickness of powder layer and a new powder layer was deposited. The melting process was repeated in this way under the protection of inert gas atmosphere in case of oxidation. Laser power, spot diameter, scanning rate and scanning line spacing powder were 85 W, 0.5 mm, 25 mm/s and 0.03 mm. The powder layer thickness was 0.08 mm in the laser melting process. After the completion of laser melting, alcohol with a purity of 99% was used to clean the Fe/CNTs composites for 3 min to remove unmelted powders. In this study, Fe powder (Shanghai Naiou Nano Technology Co. Ltd., China) with a purity of 99.5% was spherical and mean particle size was approximate 35 μm, as shown in Fig. 2(a), (c) and (d). CNTs (Beijing Boyu High Technology & New Material Co. Ltd., China) with an aspect ratio of 300–4000 were employed as the original material, as shown in Fig. 2(b). The diameter and length of CNTs ranged 5–10 nm and 3–20 μm, respectively. The electrical conductivity was > 100 s·cm−1 and specific surface area was > 500 m2·g−1.

The mechanical properties of Fe/CNTs composites were evaluated in terms of microhardness, compression strength and bending strength. Microhardness was measured using a Vickers reader (Shanghai Taiming Optical Instrument Co. Ltd., China) equipped with a diamond indenter. The surface of samples was polished by 1600 grit SiC sandpaper and subsequently loaded with a load of 0.98 N and dwell time of 10 s for microhardness tests. Specimens with a height of 5 mm and a diameter of 3 mm were fabricated to determine compression strength. According to the ASTM E9-09 standard [1], compression tests were performed using an electronic universal testing machine (Shenzhen Rambo Material Testing Co. Ltd., China) equipped with 50 kN load cell. Four independent samples were tested with a speed of 0.5 mm/min in compression tests for every group at room temperature. Compression strength of samples was calculated according to the formula (2):

σc,max = Fc,max / S

(2)

where σc, max was compression strength (MPa), Fc, max was the maximum load before fracture (N), and S was the cross-sectional area (mm2). Specimens with a dimension of 50 × 5 × 5 mm3 (in length, width and height) were prepared to evaluate the bending strength. In threepoint bending tests (Shenzhen Rambo Material Testing Co., Ltd.), the span between two supporting pins was 30 mm and the speed was 0.5 mm/min. Four repeated specimens were used for every group in the bending tests. 2.4. Degradation tests SBF was used for degradation tests, including electrochemical tests and immersion tests. The SBF with a pH of 7.4 was prepared based on the method described in the literature [26] and it was composed of NaCl 8.035 g·l−1, K2HPO4·3H2O 0.231 g·l−1, MgCl2·6H2O 0.311 g·l−1, CaCl2 0.292 g·l−1, KCl 0.225 g·l−1, Na2SO4 0.072 g·l−1, NaHCO3 0.355 g·l−1 and (CH2OH)3CNH2 6.118 g·l−1. The SBF was not buffered to record the pH changes which acted as an indicator to evaluate the degradation rate of samples. Meanwhile, the SBF was aerated since O2 would influence Fe corrosion.

2.2. Microstructural characterization To evaluate microstructural characterization of Fe/CNTs composites, all the samples were ground by SiC sandpapers and polished using a lubricant. The different phases of Fe/CNTs powders and composites were determined through X-ray diffraction meter (XRD, Rigaku Co., Tokyo, Japan). The scanning rate, accelerating voltage and current were set as 8°·min−1, 40 kV and 30 mA, respectively. With radiation source of Cu Ka, continuous X-ray diffraction spectra were recorded from 15° to 90°. Metallographic specimens of Fe/CNTs composites were etched with a 4% Nital solution for 10–20 s. The grains of Fe/CNTs composites were observed by an optical microscope (PMG-3, Olympus

2.4.1. Electrochemical tests The electrochemical tests were conducted using a three-electrode cell on an electrochemical work station (CHI660C, Shanghai Chenhua, China) in SBF at 37 °C. A platinum electrode, saturated calomel electrode (SCE) and Fe/CNTs composites acted as the counter electrode, reference electrode and working electrode, respectively. The surface 2

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

Fig. 1. Schematic view for synthesizing Fe/CNTs composites: (a) CNTs dispersion in ethanol, (b) dispersion of Fe/CNTs powders, (c) filtration and drying and (d) selective laser melting process.

area of Fe/CNTs composites exposed to 100 ml of SBF was 1 cm2, which was used to calculate the electrochemical parameters owing to the contribution of CNTs to the electrochemical reactions. The open circuit potential measurements were set for 4200 s and the electrochemical impedance spectroscopy (EIS) were carried out with the sinusoidal signal perturbation of 10−2 V and the frequency range of 10−2 to 105 Hz. The potentiodynamic polarization tests were performed at a scanning rate of 0.165 mV/s in the potential range of −1.55 V to

0.05 V. Corrosion current density (Icorr) and corrosion potential (Ecorr) were obtained according to Tafel extrapolation. Degradation rate was then computed using Eq. (3) [25]:

R = Ki

Icorr m ρ

(3)

in which R (mm·y−1) was the degradation rate, Ki was conversion coefficient of 3.27 × 10−3 (mm·g·μA−1·cm−1·y−1), Icorr (μA·cm−2) was 3

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

Fig. 2. (a) XRD patterns of Fe, Fe/0.9CNTs composite and Fe/1.2CNTs composite fabricated by SLM, as well as the original Fe powder and CNTs powder, (b) an enlarged view of XRD peaks around 26 degree and (c) Raman spectrum of Fe, Fe/0.9CNTs composite and Fe/1.2CNTs composite fabricated by SLM, as well as the original CNTs powder.

the corrosion current density, ρ (g·cm−3) was the density of samples and it was determined according to Archimedes method, m was the equivalent weight (27.92 g/eq) based on oxidation of Fe to Fe2+ [27]. Moreover, the surface morphologies of Fe/CNTs composites after potentiodynamic polarization tests were observed by SEM.

distilled water and 200 g CrO3. The samples were then kept 50 °C in incubator for 2 h. Finally, according to ASTM G31 [15], the samples were weighed and the corrosion rate in the immersion tests was determined and treated as the degradation rate (DR) on the basis of Eq. (4):

2.4.2. Immersion tests In vitro static immersion tests were performed in SBF for 7, 14, 21 and 28 days, respectively at 37 °C. Fe/CNTs composites with a diameter of 5 mm and a height of 3 mm were polished by a grinding machine, cleaned by alcohol and finally weighed by a balance with an accuracy of 0.1 mg before exposure to SBF. Four samples were used for every group. The ratio of the surface area to SBF was 0.1 cm2·ml−1 and SBF was refreshed every five days [26]. After the pre-selected period, Fe/ CNTs composites were removed from SBF, rinsed by ethanol. The corrosion products were washed by an acid solution composed of 1000 ml

DR = k

M A×T×ρ

(4)

in which, DR (mm·y−1) was the degradation rate, k was conversion coefficient of 8.76 × 104, M (g) was the weight loss, T (h) was the immersion time, A (cm2) was the exposed area and ρ (g·cm−3) was the density of Fe/CNTs composites, respectively. Besides, the surface of samples before and after removing corrosion products was observed by SEM after immersion for 28 days. Fe/CNTs composites were then cut to obtain the cross sections. Subsequently, they were mechanically polished and observed using SEM to get the corroded depth. In addition, 4

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

relative intensity, the (002) plane of Fe had the maximum intensity compared to other crystal planes, which was due to the preferential orientation during SLM. An enlarged view of these zones at about 26° was supplemented to correctly compare the different samples. It could be found that (002) peak was detected at about 26° in both the XRD patterns of Fe/1.2CNTs composite and CNTs powder, which proved the existence of CNTs. The relative weak intensity of CNTs in the composites might be attributed to the strong crystalline peak of Fe and the sharpened peak might be related to the discrete state of CNTs in the composites as compared with the aggregated state of the CNTs powder [30,31]. Besides, the (002) peak was not detected in other composites due to the relatively small amounts of CNTs. Meanwhile, there were no new compounds, for example, Fe2O3, FeO, or Fe3C etc., could be identified in the XRD patterns. These XRD results showed that chemical interactions didn't occur between Fe and CNTs during the mixing and laser melting, indicating that CNTs retained their chemical properties in the Fe/CNTs composites. When CNTs content decreased to 0.9 wt%, the diffraction peaks of CNTs were not detected because of their low content. However, the presence of CNTs was confirmed in Fe/0.9CNTs composite by Raman spectra analysis (Fig. 2(c)). The peak at 1351.13 cm−1 (D-band) corresponded to carbon atom vibration at the inplane termination of disordered graphite. The peak at 1590.63 cm−1 (G-band) was sp2 bonded carbon atom vibration in the 2D hexagonal lattice. The slight broadening of the D peak was related to the distribution of clusters with different orders and dimensions [32], indicating a slight influence on the crystallinity of CNTs during laser melting. To quantify the influence, the intensity ratios of D-band to Gband (ID/IG) were calculated to evaluate the defect density in CNTs (Fig. 2(c)). It could be found that the intensity ratios of ID/IG were 1.22 and 1.18 for Fe/0.9CNTs and Fe/1.2CNTs composites, respectively, which were close to that of the CNTs powder. Besides, the Raman spectra shift of CNTs modes towards higher cm−1 might be due to the less intertube interactions in the composites [33,34]. The results suggested that the laser melting process did not induce obvious defects on the structure of CNTs.

in the immersion tests, the pH of SBF with samples was recorded with the prolongation of time by a pH meter (IM-55G, Toa Electronics Co., Japan) with a micro glass electrode (GST-5721C, accuracy: 0.01). To obtain accurate data, measurements were repeated three times for each group and the average data was the reported value. Additionally, the roughness of corroded surface was also observed by a Wyko NT9100 optical profiling system (Veeco Instruments Inc., Plainview, America). Cross sections of Fe/CNTs composites were investigated using SEM after that the composites were dried, embedded and polished. 2.5. Cytocompatibility tests Osteoblast-like MG-63 cell culture tests were carried out to evaluate effects of Fe/CNTs composites on cytocompatibility. The cells were obtained from Shanghai Cellular Biology Institute and cultured in Dulbecco's modified Eagle's medium (DMEM) at 37 °C with 5% CO2. The DMEM contained 1% penicillin/streptomycin and 10% fetal bovine serum. Cytocompatibility tests were performed by indirect contact method. Fe/CNTs composites were sanitized using ethanol three times, treated with ultraviolet light sterilization for 20 min and lastly soaked for 3 days in DMEM to obtain extracts. According to ISO10993-12, the surface area of sample to DMEM was 1.25 cm2·ml−1 [15]. The extracts were first centrifuged to obtain supernatant fluid, which was subsequently stored at 4 °C for cytocompatibility tests. The cells were incubated for 4 h in DMEM using a 24-well plate. Then, the cell culture medium was replaced by extracts of Fe/CNTs composites. At the same time, DMEM was used for control group. The cells were incubated in a humidified atmosphere for 1, 2 and 3 days, respectively. Lastly, Ethidium homodimer-1 and Calcein-AM reagents were used to stain the cells for 15 min. Fluorescence images of MG-63 could be obtained through a fluorescence microscopy (Olympus BX60, Japan). For cell viability tests, MG-63 Cells were fostered for 24 h in the 96well plate at seeding density of 1 × 103 cells/100 μl DMEM. Subsequently, DMEM was replaced by the extracts of Fe/CNTs composites, respectively. At the same time, DMEM was used as control group. After culture in an incubator with 5% CO2 for 1, 2 and 3 days, respectively, 10 μL cell counting kit (CCK-8) was added to the 96-well plate. Thereafter, the absorbance was obtained by a microplate reader. According to ISO 19003-544 [15], cell viability was calculated based on the formula (5):

C = OD1/ OD2 %

3.2. Microstructural characteristics Optical micrographs and average grain sizes of Fe/CNTs composites were shown in Fig. 3. Clearly, Fe was composed of coarse grain with an average grain size of 39 μm. With the addition of 0.3 and 0.6 wt% CNTs, the average grains continuously reduced to 30 and 18 μm, respectively. In Fe/0.9CNTs composite, the grains were remarkably refined to 12 μm. It could be concluded that the addition of CNTs refined the grain sizes of Fe because that fine profile of CNTs restricted grain growth. Meanwhile, CNTs were dispersed on grain boundaries, which was similar to the reports in the literature [35]. This distribution of CNTs might lead to intergranular corrosion, which could, under severe conditions, led to grain-dropping [36]. However, the grain sizes were not decreased significantly when further increasing CNTs content to 1.2 wt%. Besides, the relative densities of Fe/CNTs composites were 96.4% (Fe), 95.8% (Fe/0.3CNTs), 94.2% (Fe/0.6CNTs), 93.9% (Fe/0.9CNTs) and 88.5% (Fe/1.2CNTs), indicating that the relative densities decreased with the increase of CNTs. And some large pores were observed in the Fe/ 1.2CNTs composite (Fig. 3), which were ascribed to excessive CNTs hindered the bonding of liquid phase Fe. Thus, the relative density was dramatically decreased.

(5)

in which, C was cell viability, OD1 and OD2 were the mean absorbance of experimental sample and control group, respectively. 2.6. Statistical analysis Data in this study were expressed as mean ± standard deviations. One-way ANOVA was used to analyze statistical significance between two groups and difference was thought to be significant when p < 0. 05 (*) or p < 0.01 (**). 3. Results and discussion 3.1. Phase characteristics XRD patterns of Fe, Fe/0.3CNTs composite, Fe/0.6CNTs composite Fe/0.9CNTs composite and Fe/1.2CNTs composite fabricated by SLM, as well as the original Fe powder and CNTs powder were shown in Figs. 2 and S2. It could be found that the peaks of Fe and CNTs were observed in the XRD pattern of Fe/1.2CNTs composite. The peaks of CNTs showed orientations of (002) and (100) which were consistent with those reported in ZnO incorporated CNTs by Kennedy et al. [28,29]. It could be seen that no significant difference in peak intensity was observed among Fe and Fe/CNTs composites. From the view of

3.3. Degradation characteristics 3.3.1. Electrochemical tests The open circuit potentials (OCP) of Fe/CNTs samples in SBF were shown in Fig. 4(a). It was found that Fe/0.9CNTs and Fe/1.2CNTs samples exhibited lower values than of Fe, indicating a poor passivation on sample surface after incorporation of CNTs. The potentiodynamic polarization curves of Fe/CNTs composites were presented in Fig. 4(b). 5

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

Fig. 3. Optical micrographs and average grain sizes of Fe/CNTs composites: (a) Fe, (b) Fe/0.3CNTs, (c) Fe/0.6CNTs, (d) Fe/0.9CNTs and (e) Fe/1.2CNTs.

The corrosion potential (Ecorr) and corrosion current densities (Icorr) of Fe/CNTs composites were obtained according to Tafel extrapolation, as displayed in Table 1. Obviously, the Ecorr (vs. SCE) of Fe/CNTs composites could be ranked as Fe/0.3CNTs (−0.595 V) > Fe/0.6CNTs (−0.628 V) > Fe/0.9CNTs (−0.683 V) > Fe/1.2CNTs (−0.712 V). All the CNTs containing composites exhibited lower Ecorr than that of Fe (−0.533 V), which indicated that Fe became prone to corrosion. In this study, it was worth noting that the more amount of CNTs were included in the composite, the more amount of active sites near the Fe-CNTs interface were introduced and then the corrosion rate of the composite was enhanced with the increase of CNTs contents. In this case, because the anodic reaction rate on the Fe increased, the corrosion potential presented a shift towards the negative direction with the increase of CNT concentration. Similar phenomena have been reported in the literature [37–39], where the composites containing noble phases, such as Au, Ag, Pd, Pt, etc., exhibited more negative potentials than Fe in galvanic corrosion. Meanwhile, the Icorr of Fe was 6.209 μA·cm−2, and Icorr increased from 7.284 for Fe/0.3CNTs composite to 12.831 μA·cm−2

for Fe/0.6CNTs composite. With CNTs content further increasing to 0.9 and 1.2 wt%, the Icorr increased to 17.549 and 19.950 μA·cm−2, respectively. It was well accepted that the degradation rate was positively related to Icorr [40,41]. The calculated degradation rate increased from 0.088 to 0.241 mm·y−1, as shown in Fig. 4(c). An equivalent circuit model [Rs(CPE1‐Rt)] was employed to fit the EIS data of all the samples(Fig. 4(d)). This model was commonly employed to describe the corrosion behavior of Fe-based implants [37,42]. The parameters Rt and Rs in the circuit represented the polarization resistance and electrolyte resistance, respectively. CPE1 represented a constant phase element, which was considered to be the nonideal capacitive behavior of the electric double layers owing to the dislocations, impurities and grain boundaries, etc. [43]. Moreover, the Nyquist plots were shown in Fig. 4(d), in which a series of semicircles about the excitation frequency impedance imaginary part (−Z″) as a function of the impedance real part (Z′) were obtained. It was found that the diameters of semicircles were smaller with the increasing content of CNTs, showing their worse corrosion resistance. Since the diameters of 6

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

Fig. 4. Electrochemical tests of Fe/CNTs composites in SBF at 37 °C: (a) open circuit potentials, (b) potentiodynamic polarization curves, (c) corrosion rates based on extrapolating polarization curves and (d) Nyquist plots.

Fig. 5(e) and the size of corrosion pits was approximately 2–5 μm in large magnification SEM image of Fe/1.2CNTs composite (Fig. 5(f)). Pitting corrosion might be due to the uneven distribution of excessive carbon nanotubes (1.2 wt%). Pitting corrosion might be due to the uneven distribution of excessive carbon nanotubes (1.2 wt%), which caused severe corrosion. Small cavities or holes might happen during long-term degradation in the physiological environment, which caused a great deal of damage to bone repair. Since corrosion was closely related to the composition of Fe/CNTs composites [44], the corrosion behavior could be interpreted from the following two aspects. On the one hand, CNTs possessed a higher corrosion potential (+0.22 V) than Fe (−0.414 V). And thus multi-phases with corrosion potential difference coexisted on the surface, accelerating the degradation of Fe through galvanic corrosion between Fe and CNTs. On the other hand, the corrosion became more seriously with the increase of CNTs, which was due to the large specific surface area and excellent electrical conductivity of CNTs, thus increasing increase area ratios of cathode to anode, lowering electrical resistance of cathode and thereby increasing the corrosion current density. Ecorr and Icorr were extracted from the intercept of Tafel slopes using Tafel extrapolation method (Fig. S5) and were summarized in Table S1. It could be found that Ecorr of samples from high to low was Fe, Fe/0.3CNTs, Fe/0.6CNTs, Fe/0.9CNTs, Fe/1.2CNTs composites. This exhibited the same trend with that in Table 1. Moreover, Ecorr of Fe/CNTs composites and Fe were lower compared with the corresponding values in Table 1, which was due to accumulation of corrosion products with more negative potentials. Meanwhile, Icorr of Fe/CNTs composites were 1.25, 1.91, 2.58, 2.72 times of Fe. This indicated that Fe/CNTs composites had a greater corrosion tendency compared with Fe even after long term of immersion.

Table 1 Electrochemical parameters of Fe/CNTs composites extracted from Tafel polarization curves. Materials

Ecorr (V)

Fe Fe/0.3CNTs Fe/0.6CNTs Fe/0.9CNTs Fe/1.2CNTs

−0.533 −0.595 −0.628 −0.683 −0.712

Icorr (μA·cm−2) ± ± ± ± ±

0.042 0.039 0.043 0.051 0.057

6.21 ± 0.37 7.28 ± 0.58 12.83 ± 0.79 17.55 ± 0.94 19.95 ± 1.02

semicircles were considered to be the polarization resistance and thereby smaller polarization resistance corresponded to faster corrosion. Besides, it can be found from Bode plots (Fig. S4) that there was a flat portion of curves (slope was nearly 0) in the high frequency of approximate 102–105 Hz and the phase angle dropped towards zero degree in the high frequency of Bode phase plots. This was attributed to the response of electrolyte resistance. In the middle and low frequency, Fe/CNTs composites, especially Fe/0.9 CNTs and Fe/1.2 CNTs composites, showed both lower impedance and phase angles than Fe. This suggested a greater tendency to corrosion after addition of CNTs. These results showed that the degradation of Fe was accelerated due to addition of CNTs and the degradation rate increased with the increase in CNTs contents. The surface morphologies of Fe/CNTs composites after potentiodynamic polarization tests in SBF were depicted in Fig. 5(a)–(f). For Fe, the surface remained relatively even and intact, as shown in Fig. 5(a). For Fe/0.3CNTs composite, corrosion products appeared on the surface after polarization tests, as shown in Fig. 5(b). Compared with Fe, the corrosion of Fe/0.6CNTs and Fe/0.9CNTs composites were intensified in SBF and a great many of plate-like corrosion products precipitated on the surface, especially Fe/0.9CNTs composite, as shown in Fig. 5(c–d). For Fe/1.2CNTs composite, severe pitting corrosion was observed in

3.3.2. Immersion tests The morphologies of Fe/CNTs composites after immersion for 7

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

Fig. 5. SEM images of the surface morphology after potentiodynamic polarization tests in SBF (a) Fe, (b) Fe/0.3CNTs composite, (c) Fe/0.6CNTs composite, (d) Fe/ 0.9CNTs composite, (e) Fe/1.2CNTs composite and (f) large magnification SEM image of Fe/1.2CNTs composite.

mechanical properties after degradation was an important research direction of Fe-based implants. Chemical compositions of corrosion products were analyzed by EDS, and the results indicated the major presence of Fe, C and O elements (Fig. 7(c)), which was in accordance with other studies [16,46,47]. It was worth noting that small amounts of Ca and P elements were detected, which was beneficial to promote bone healing because that Ca and P elements were important components of natural bone [48,49]. The degradation rates of Fe/CNTs composites were presented in Fig. 7(e). The degradation rate of Fe was 0.085 mm·y−1. After adding CNTs, degradation rates were 0.095, 0.102, 0.148 and 0.152 mm·y−1 for Fe/0.3CNTs, Fe/0.6CNTs, Fe/0.9CNTs and Fe/1.2CNTs composites, increasing by 12%, 20%, 74%, 79%, respectively. The pH of immersion solution was also evaluated, as shown in Fig. 7(f). With the increase of CNTs contents, the pH continually increased due to the released OH− caused by the corrosion of Fe [50], which was in line with the trend of degradation rate. Illustration of corrosion mechanisms after adding CNTs was shown in Fig. 7(g)–(i). Owing to the differences in corrosion potential, the corrosion process of Fe/CNTs composites occurred through a series of anode and cathode reactions, as shown in Fig. 7(g). Fe matrix acted as anodes and the anodic reaction was the dissolution of Fe according to formula (6) [50]:

28 days in SBF were presented in Figs. 6(a–b) and (a–c). Obviously, Fe didn't suffer severe corrosion with corrosion products accumulating on partial surface. The surface of Fe/0.3CNTs composite was roughly similar to that of Fe. Fe/0.6CNTs and Fe/0.9CNTs composites showed different surface morphology in comparison with Fe. Original surface were almost invisible and dense corrosion products covered on their surface, especially Fe/0.9CNTs composite. As for Fe/1.2CNTs composite, dense corrosion products also formed on the surface while corrosion holes with size about 15 μm could be found due to non-uniform corrosion [45]. The morphologies of Fe/CNTs composites after the removal of corrosion products were exhibited in in Figs. 6(c–d) and S6(d–f). It could be found that although there was a small amount of corrosion product elements C and O, the majority element on the surface was Fe from matrix, as shown in Fig. S6(g). The surface of Fe presented shallow and fine corrosion pits. The surface of Fe/0.3CNTs composite became serious, suggesting that adding small content of CNTs could accelerate corrosion of Fe. As for Fe/0.6CNTs and Fe/ 0.9CNTs composites, the corrosion became more intensely and almost no localized corrosion could be observed, especially Fe/0.9CNTs composites. With the content of CNTs further increasing to 1.2 wt%, severe corrosion cracks occurred due to localized corrosion. The cross sections of Fe/CNTs composites after immersion for 28 days in SBF were presented in Figs. 7(a–b) and S7. There was a clear distinction between matrix and the corrosion products. The corrosion products had a dense character in the case of Fe samples, as shown in Fig. 7(a). For Fe/0.3CNTs, Fe/0.6CNTs, Fe/0.9CNTs, Fe/1.2CNTs composites, the corrosion products became thicker and more porous. Their corrosion product depth was approximately 24, 32, 50 and 55 μm, respectively, which was thicker than that of Fe (17 μm) (Fig. 7(d)). For Fe/1.2CNTs composites, intergranular corrosion might take place as a result of addition of excessive CNTs, causing a reduction in strength, ductility and ultimately structural integrity. Therefore, the study of

Fe → Fe2 + + 2e−

(6)

The occurrence of galvanic corrosion is determined by potential, which is a necessary condition for galvanic corrosion. The extent of galvanic corrosion depends on various factors, including the electrical resistance of the galvanic cell, the area ratio of cathode to anode, and solution temperature, etc. [51]. Schneider et al. reported that galvanic corrosion was determined not only by the potential difference, but moreover by the cathodic process (oxygen reduction), which was 8

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

Fig. 6. Corrosion morphologies after immersion in SBF for 28 days: (a) Fe, (b) Fe/1.2CNTs composite; surface morphologies after removal of corrosion products (c) Fe, (d) Fe/1.2CNTs composite.

2H2 O + O2 + 4e− → 4OH−

2+

Fe3 + + 3OH− → Fe(OH)3 ↓

(9)

PO33−,

2PO43 − + 3Ca2 + → Ca3 (PO4 )2 ↓

(11)

2PO43 − + 3Fe2 + + 8H2 O → Fe3 (PO4 )2 ·8H2 O↓

(12)

PO43 − + Fe3 + → FePO4 ↓

(13)

This was the formation mechanisms of Ca and P elements in the corrosion products. 3.4. Mechanical properties

The enhanced cathodic reactions would accelerate the dissolution of Fe at the anodic according to the mixed potential theory [53]. With the further degradation, Fe(OH)2 formed on account of the reaction between OH− and Fe2+. Simultaneously, other corrosion produces also appeared on the Fe/CNTs composite surface during the degradation process according to formulae (8)–(10) [50], as shown in Fig. 7(i): (8)

HPO32−

SBF was a solution containing Ca , and etc. The corrosion of Fe/CNTs led to the increase in pH, which promoted the precipitation and deposition of phosphates as follows:

(7)

Fe2 + + 2OH− → Fe(OH)2

(10)

Fe(OH)2 + 2Fe(OH)3 → Fe3 O4 ↓ + 4H2 O

charge transfer controlled and depended on the electrical conductivity of the cathode [21]. Generally, high electrical conductivity brings about low electrical resistance of cathode in galvanic cell and allows significant levels of electron transfer through the cathode, thereby resulting in a high corrosion current density [52]. In this study, the large specific surface area of CNTs could create maximum contact area. This increased the area ratios of cathode to anode, which accelerated the degradation of Fe. More importantly, the excellent electrical conductivity of CNTs lowered the electrical resistance when electrons (e−) from the dissolving Fe transferred through the cathode, as shown in Fig. 7(h), thereby increasing corrosion current density. Thus, O2 at the cathode could easily and quickly obtain the electrons and cathodic reactions occurred based on the formula (7):

The microhardness, compression strength and bending strength of the Fe/CNTs composites were presented in Figs. 8 and S8(a). It could be found that the microhardness gradually increased with CNTs content increasing from 0.3 to 0.9 wt%, as shown in Fig. 8(a). For Fe/1.2CNTs composite, the microhardness decreased due to the uncompacted microstructure with large pores, as shown in Fig. 3(e). At the same time, indentation cracks had occurred for Fe/1.2CNTs composite in Fig. S8(b), indicating a potential implantation failure [54]. Compression strength was another indicator for bone implants [1]. 9

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

Fig. 7. Cross sections of (a) Fe, (b) Fe/1.2CNTs composite, respectively; (c) EDS elemental analysis of area A; (d) corroded depth after immersion in SBF for 28 days, (e) degradation rates and (f) pH changes in SBF against time of Fe/CNTs composites; Illustration of corrosion mechanisms: (g) initial corrosion stage, (h) partial enlargement perspective view of cathodic reaction and (i) stable corrosion stage with corrosion products on the surface.

defined 3 days later. The cells in extracts of Fe/CNTs composites showed no obvious difference in distribution and morphology, suggesting that the incorporation of CNTs into Fe didn't exert a harmful impact on cell morphology comparing with that of control group. Moreover, the MG-63 cell proliferation in extracts of Fe/CNTs composites was investigated by CCK-8 assays and the cell viability (Fig. 9) were obtained according to the report on Zinc oxide doped TiO2 nanocrystals by Kaviyarasu et al., in which graphs were plotted using the sample at X-axis and % of cell viability at Y-axis [58]. Cell viability reflected cell proliferation, which was widely used [59,60]. It could be seen that all the extracts supported the cell proliferation with the increase of time. As compared with control group, Fe, Fe/0.3CNTs, Fe/ 0.6CNTs and Fe/0.9CNTs composites exhibited a stimulatory effect on the cell proliferation, even a further addition of CNTs to 1.2% showing no pronounced inhibitory action with the prolonged incubation. Cell viability was 95% for Fe, 94% for Fe/0.3CNTs, 93% for Fe/0.6CNTs, 91% for Fe/0.9CNTs and 88% for Fe/1.2CNTs, respectively, after incubation for 3 days, which was much higher than 75%, a criterion of good cytocompatibility [1]. The increasing toxicity with the increased CNTs content could be

The compression yield strength of Fe/CNTs composites was summarized in Fig. 8(b). Fe/0.3CNTs, Fe/0.6CNTs, Fe/0.9CNTs and Fe/ 1.2CNTs composites exhibited high compression strength of 180, 190, 220 and 210 MPa, respectively, in comparison with Fe (175 MPa). It could be found that CNTs (0.3–0.9 wt%) improved the compression yield strength of Fe, which would provide sufficient mechanical support for human compact bone to resist flexural load after implantation [54]. The improved compression yield strength was owing to the refinement of grains, which increased the number of grain boundary, effectively restricting movement of dislocation [55,56]. As for the bending strength of Fe/CNTs composites, it showed a similar trend with compression strength, as shown in Fig. 8(c).

3.5. Cytocompatibility studies Biocompatibility was essential for the orthopedic applications of composites [57]. In the present study, MG-63 cell morphologies in extracts of Fe/CNTs composites were evaluated by fluorescence images and the results were presented in Fig. S9. It could be found that all the extracts supported cell growth and the cell morphology was well10

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

Fig. 8. (a) Line charts based on random microhardness tests, (b) compression strength and (c) bending strength of Fe/CNTs composites.

implants should possess a degradation rate of approximate 0.5 mm·y−1 [66]. Actually, Fe had a too slow degradation process in physiological environment in spite of its high mechanical properties [67]. Thus, Febased bone implants with enhanced degradation rates were urgently needed [68]. In this study, noble potential CNTs with large specific surface area and excellent electrical conductivity were added into Fe to induce a large number of galvanic corrosion cells, strongly enhancing the corrosion rate of Fe. Consequently, Fe/0.9CNTs composite and Fe/ 1.2CNTs composite showed high degradation rates among Fe/CNTs composites while Fe/0.9CNTs composite exhibited no severe corrosion holes or cracks as a result of uniform corrosion. Besides, mechanical properties should also be taken into account when developing Fe-based implants, especially in the field of load-bearing orthopedics. Fe/ 0.9CNTs composite with fine and uniform microstructure improved mechanical properties and provided sufficient mechanical support for bone repair [27]. On the contrary, Fe/1.2CNTs presented a microstructure comprising large pores, which led to the deterioration of mechanical properties, for instance, the formation of indentation cracks in the microhardness tests. As a result, this was directly brought about early failure of orthopedic implant. In terms of biocompatibility, the cell viability of Fe/0.9CNTs composite was higher than that of Fe/ 1.2CNTs composite, indicating a better cytocompatibility. Therefore, it could be concluded that Fe/0.9CNTs composite might be a promising candidate for use as bone implants owing to the combination of enhanced degradation rates, favorable mechanical properties and good cytocompatibility.

Fig. 9. Cell viability of MG-63 cells after incubation for 1, 2, 3 days, respectively.

attributed to the higher degradation rates which resulted from more severe galvanic corrosion. On the one hand, compared with Fe, the accelerated degradation would inevitably lead to more release of Fe ions, which has been reported to have some inhibitory effects on cell viability [61]. On the other hand, the accelerated degradation caused rapid increase of local pH value, which may also inhibit cell viability [62–65]. As for the long-term degradation process of the composite, degradation products would gradually cover on the matrix with the prolongation of time. This inevitably hindered the invasion of corrosive medium to some extent. As a result, the degradation rate would be maintained at a stable value, as well as the pH (Fig. 7(f)). The in vitro cell culture results showed that cell viability continually increased with increasing culture time, indicating improved cytocompatibility of the Fe/CNTs composites after long-term degradation. Moreover, the metabolic process in the human body could further reduce the toxicity caused by the released ions and pH increase. Therefore, the cytocompatibility of the composites would be improved during the longterm degradation process. It was generally known that the recovery period of bone tissue ranged from 3 to 12 months, which demanded that biodegradable

4. Conclusions A series of Fe/xCNTs (x = 0, 0.3, 0.6, 0.9, 1.2 wt%) composites were fabricated by selective laser melting to assess their feasibility for use as degradable load-bearing bone implants. It was revealed that degradation rates increased by 12% for Fe/0.3CNTs composite, 20% for Fe/0.6CNTs composite, 74% for Fe/0.9CNTs composite and 79% for Fe/1.2CNTs composite, respectively, due to the enhanced corrosion induced by CNTs with noble potential, large specific surface area and excellent electrical conductivity. Moreover, the composites exhibited accelerated corrosion at CNTs level ranging from 0.3 to 0.9 wt% while excessive addition of CNTs led to corrosion holes and cracks due to localized corrosion. Meanwhile, the addition of CNTs improved the mechanical properties, whereas an excessive addition of CNTs indeed caused the deterioration of mechanical properties. In addition, all the 11

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

Fe/CNTs composites exhibited good cytocompatibility in MG-63 cell culture tests.

[20]

Acknowledgments

[21] [22]

This study was supported by the following funds: (1) The Natural Science Foundation of China (51705540, 81871494, 81871498); (2) Hunan Provincial Natural Science Foundation of China (2018JJ3671, 2019JJ50588); (3) Guangdong Province Higher Vocational Colleges & Schools Pearl River Scholar Funded Scheme (2018); (4) The Open Sharing Fund for the Large-scale Instruments and Equipments of Central South University; (5) The Project of Hunan Provincial Science and Technology Plan (2017RS3008); (6) Shenzhen Science and Technology Plan Project (JCYJ20170817112445033); (7) National Postdoctoral Program for Innovative Talents (BX201700291); (8) The China Postdoctoral Science Foundation (2018M632983).

[23]

[24]

[25]

[26] [27]

Appendix A. Supplementary data

[28]

Supplementary data to this article can be found online at https:// doi.org/10.1016/j.msec.2019.109935.

[29]

References

[30]

[1] S. Wang, Y. Xu, J. Zhou, H. Li, J. Chang, Z. Huan, Invitro degradation and surface bioactivity of iron-matrix composites containing silicate-based bioceramic, Bioactive Materials 2 (2017) 10–18. [2] C. Gao, S. Peng, P. Feng, C. Shuai, Bone biomaterials and interactions with stem cells, Bone Res 5 (2017) 17059. [3] C. Shuai, W. Guo, P. Wu, W. Yang, S. Hu, Y. Xia, P. Feng, A graphene oxide-Ag codispersing nanosystem: dual synergistic effects on antibacterial activities and mechanical properties of polymer scaffolds, Chem. Eng. J. 347 (2018) 322–333. [4] J. Čapek, Š. Msallamová, E. Jablonská, J. Lipov, D. Vojtěch, A novel high-strength and highly corrosive biodegradable Fe-Pd alloy: structural, mechanical and in vitro corrosion and cytotoxicity study, Mater. Sci. Eng. C 79 (2017) 550–562. [5] C. Shuai, Y. Xu, P. Feng, G. Wang, S. Xiong, S. Peng, Antibacterial polymer scaffold based on mesoporous bioactive glass loaded with in situ grown silver, Chem. Eng. J. 374 (2019) 304–315. [6] J. Hufenbach, F. Kochta, H. Wendrock, A. Voß, L. Giebeler, S. Oswald, S. Pilz, U. Kühn, A. Lode, M. Gelinsky, S and B microalloying of biodegradable Fe-30Mn-1C - effects on microstructure, tensile properties, in vitro degradation and cytotoxicity, Mater. Design 142 (2018) 22–35. [7] D.T. Chou, D. Wells, D. Hong, B. Lee, H. Kuhn, P.N. Kumta, Novel processing of iron-manganese alloy-based biomaterials by inkjet 3-D printing, Acta Biomater. 9 (2013) 8593–8603. [8] P. Feng, P. Wu, C. Gao, Y. Yang, W. Guo, W. Yang, C. Shuai, A multimaterial scaffold with tunable properties: toward bone tissue repair, Advanced Science 5 (2018) 1700817. [9] Y. Yang, J. Zhou, R. Detsch, N. Taccardi, S. Heise, S. Virtanen, A.R. Boccaccini, Biodegradable nanostructures: degradation process and biocompatibility of iron oxide nanostructured arrays, Mater. Sci. Eng. C 85 (2018) 203–213. [10] P. Feng, J. He, S. Peng, C. Gao, Z. Zhao, S. Xiong, C. Shuai, Characterizations and interfacial reinforcement mechanisms of multicomponent biopolymer based scaffold, Mater. Sci. Eng. C 100 (2019) 809–825. [11] C. Shuai, J. Zan, F. Qi, G. Wang, Z. Liu, Y. Yang, S. Peng, nMgO-incorporated PLLA bone scaffolds: enhanced crystallinity and neutralized acidic products, Mater. Design 174 (2019) 107801. [12] C. Shuai, Y. Li, G. Wang, W. Yang, S. Peng, P. Feng, Surface modification of nanodiamond: toward the dispersion of reinforced phase in poly-l-lactic acid scaffolds, Int. J. Biol. Macromol. 126 (2019) 1116–1124. [13] C. Shuai, Y. Cheng, Y. Yang, S. Peng, W. Yang, F. Qi, Laser additive manufacturing of Zn-2Al part for bone repair: formability, microstructure and properties, J. Alloys Compd. 798 (2019) 706–715. [14] J. Čapek, K. Stehlíková, A. Michalcová, Š. Msallamová, D. Vojtěch, Microstructure, mechanical and corrosion properties of biodegradable powder metallurgical Fe-2 wt % X (X=Pd, Ag and C) alloys, Mater. Chem. Phys. 181 (2016) 501–511. [15] T. Huang, J. Cheng, D. Bian, Y. Zheng, Fe–Au and Fe–Ag composites as candidates for biodegradable stent materials, J. Biom. Mater. Res. B 104 (2016) 225–240. [16] T. Huang, J. Cheng, Y.F. Zheng, In vitro degradation and biocompatibility of Fe-Pd and Fe-Pt composites fabricated by spark plasma sintering, Mater. Sci. Eng. C 35 (2014) 43–53. [17] A. Dasari, Z.Z. Yu, Y.W. Mai, Electrically conductive and super-tough polyamidebased nanocomposites, Polymer 50 (2009) 4112–4121. [18] A. Moisala, Q. Li, I.A. Kinloch, A.H. Windle, Thermal and electrical conductivity of single- and multi-walled carbon nanotube-epoxy composites, Comp. Sci. Tech. 66 (2006) 1285–1288. [19] H.M. Kim, K. Kim, S.J. Lee, J. Joo, H.S. Yoon, S.J. Cho, S.C. Lyu, C.J. Lee, Charge transport properties of composites of multiwalled carbon nanotube with metal

[31]

[32]

[33] [34]

[35]

[36]

[37]

[38]

[39]

[40]

[41]

[42]

[43]

[44]

[45]

[46]

[47]

[48]

12

catalyst and polymer: application to electromagnetic interference shielding, Curr. Appl. Phy. 4 (2004) 577–580. G. Mon, R. Ross, Electrochemical degradation of amorphous-silicon photovoltaic modules, 18th IEEE PVSC, 1985, pp. 1142–1149. M. Schneider, K. Kremmer, C. Lämmel, K. Sempf, M. Herrmann, Galvanic corrosion of metal/ceramic coupling, Corros. Sci. 80 (2014) 191–196. S.L. Edwards, J.S. Church, J.A. Werkmeister, J.A. Ramshaw, Tubular micro-scale multiwalled carbon nanotube-based scaffolds for tissue engineering, Biomaterials 30 (2009) 1725–1731. Y. Yang, F. Yuan, C. Gao, P. Feng, L. Xue, S. He, C. Shuai, A combined strategy to enhance the properties of Zn by laser rapid solidification and laser alloying, J Biom Mater Res. B 82 (2018) 51–60. C. Gao, P. Feng, S. Peng, C. Shuai, Carbon nanotubes, graphene and boron nitride nanotubes reinforced bioactive ceramics for bone repair, Acta Biomater. 61 (2017) 1. C. Shuai, L. Xue, C. Gao, Y. Yang, S. Peng, Y. Zhang, Selective laser melting of Zn–Ag alloys for bone repair: microstructure, mechanical properties and degradation behaviour, Virtual & Physical Prototyping (2018) 1–9. T. Kokubo, H. Takadama, How useful is SBF in predicting in vivo bone bioactivity, Biomaterials 27 (2006) 2907–2915. P. Sotoudehbagha, S. Sheibani, M. Khakbiz, S. Ebrahimi-Barough, H. Hermawan, Novel antibacterial biodegradable Fe-Mn-Ag alloys produced by mechanical alloying, Mater. Sci. Eng. C (2018) 88. J. Kennedy, F. Fang, J. Futter, J. Leveneur, P. Murmu, G. Panin, T. Kang, E. Manikandan, Synthesis and enhanced field emission of zinc oxide incorporated carbon nanotubes, Diam. Relat. Mater. 71 (2017) 79–84. K. Kaviyarasu, G.T. Mola, S. Oseni, K. Kanimozhi, C.M. Magdalane, J. Kennedy, M. Maaza, ZnO doped single wall carbon nanotube as an active medium for gas sensor and solar absorber, J. Mater. Sci. Mater. Electron. 30 (2019) 147–158. K.-C. Chang, C.-Y. Li, C.-K. Hsu, M.-S. Kuo, Synthesis and properties of Fe-modified calcium-deficient hydroxyapatite nanocrystal for MRI contrast agent, Biomedical Engineering: Applications, Basis and Communications 23 (2011) 393–401. T. Al Mgheer, F.H. Abdulrazzak, Oxidation of multi-walled carbon nanotubes in acidic and basic Piranha mixture, Frontiers in Nanoscience and Nanotechnology (2016) 155–158. X. Cui, W. Wei, W. Chen, Lengthening and thickening of multi-walled carbon nanotube arrays grown by chemical vapor deposition in the presence and absence of water, Carbon 48 (2010) 2782–2791. L. Bokobza, J. Zhang, Raman spectroscopic characterization of multiwall carbon nanotubes and of composites, Express Polym Lett 6 (2012). M.P. Neupane, S. Lee, J. Kang, I.S. Park, T.S. Bae, M.H. Lee, Surface characterization and corrosion behavior of silanized magnesium coated with graphene for biomedical application, Mater. Chem. Phys. 163 (2015) 229–235. J. Cheng, Y.F. Zheng, In vitro study on newly designed biodegradable Fe-X composites (X = W, CNT) prepared by spark plasma sintering, J. Biom. Mater. Res. Part B. 101B (2013) 485–497. E.M. Lehockey, G. Palumbo, P. Lin, A.M. Brennenstuhl, On the relationship between grain boundary character distribution and intergranular corrosion, Scripta Mater 36 (1997) 1211–1218. C. Shuai, C. He, P. Feng, W. Guo, C. Gao, P. Wu, Y. Yang, S. Bin, Biodegradation mechanisms of selective laser-melted Mg–xAl–Zn alloy: grain size and intermetallic phase, Virtual & Physical Prototyping 13 (2017) 1–11. X. Li, Z. Yu, H. Liu, S. Hong, Y. Leng, Biocompatibility of pure iron: In vitro assessment of degradation kinetics and cytotoxicity on endothelial cells, Mater. Sci. Eng. C 29 (2009) 1589–1592. J. Cheng, Y. Zheng, In vitro study on newly designed biodegradable Fe-X composites (X = W, CNT) prepared by spark plasma sintering, J. Biom. Mater. Res. Part B. 101 (2013) 485–497. C. Shuai, Y. Yang, P. Wu, X. Lin, Y. Liu, Y. Zhou, P. Feng, X. Liu, S. Peng, Laser rapid solidification improves corrosion behavior of Mg-Zn-Zr alloy, J. Alloys Comp. 691 (2017) 961–969. C. Shuai, B. Wang, Y. Yang, S. Peng, C. Gao, 3D honeycomb nanostructure-encapsulated magnesium alloys with superior corrosion resistance and mechanical properties, Comp. B. Eng. 162 (2019) 611–620. D. Carluccio, M. Bermingham, D. Kent, A.G. Demir, B. Previtali, M.S. Dargusch, Comparative study of pure iron manufactured by selective laser melting, laser metal deposition, and casting processes, Adv. Eng. Mater. 12 (2019) 103–112. C. Vasilescu, P. Drob, E. Vasilescu, I. Demetrescu, D. Ionita, M. Prodana, S. Drob, Characterisation and corrosion resistance of the electrodeposited hydroxyapatite and bovine serum albumin/hydroxyapatite films on Ti–6Al–4V–1Zr alloy surface, Corros. Sci. 53 (2011) 992–999. H. Wang, Y. Zheng, J. Liu, C. Jiang, Y. Li, In vitro corrosion properties and cytocompatibility of Fe-Ga alloys as potential biodegradable metallic materials, Mate. Sci. Eng. C. 71 (2017) 60–66. E. Zhang, L. Yang, J. Xu, H. Chen, Microstructure, mechanical properties and biocorrosion properties of Mg–Si(–Ca, Zn) alloy for biomedical application, Acta Biomater. 6 (2010) 1756–1762. Ä.a. J, s.J. Kubã, D. Vojtä›Ch, E. Jablonskã, J. Lipov, T. Ruml, Microstructural, mechanical, corrosion and cytotoxicity characterization of the hot forged FeMn30(wt.%) alloy, Mater. Sci. Eng. C Mater. Biol. Appl., 58 (2016) 900–908. B. Wegener, B. Sievers, S. Utzschneider, P. Müller, V. Jansson, S. Rößler, B. Nies, G. Stephani, B. Kieback, P. Quadbeck, Microstructure, cytotoxicity and corrosion of powder-metallurgical iron alloys for biodegradable bone replacement materials, Mater. Sci. Eng. B 176 (2011) 1789–1796. Y. Deng, Y. Yang, C. Gao, P. Feng, W. Guo, C. He, J. Chen, C. Shuai, Mechanism for corrosion protection of β-TCP reinforced ZK60 via laser rapid solidification, Mater.

Materials Science & Engineering C 104 (2019) 109935

C. Shuai, et al.

method, Mater. Sci. Eng. C 74 (2017) 325–333. [59] C.M. Magdalane, K. Kaviyarasu, A. Raja, M. Arularasu, G.T. Mola, A.B. Isaev, N.A. Al-Dhabi, M.V. Arasu, B. Jeyaraj, J. Kennedy, Photocatalytic decomposition effect of erbium doped cerium oxide nanostructures driven by visible light irradiation: investigation of cytotoxicity, antibacterial growth inhibition using catalyst, J. Photochem. Photobiol. B Biol. 185 (2018) 275–282. [60] A.M. Amanulla, S.J. Shahina, R. Sundaram, C.M. Magdalane, K. Kaviyarasu, D. Letsholathebe, S. Mohamed, J. Kennedy, M. Maaza, Antibacterial, magnetic, optical and humidity sensor studies of β-CoMoO4-Co3O4 nanocomposites and its synthesis and characterization, J. Photochem. Photobiol. B Biol. 183 (2018) 233–241. [61] E. Zhang, H. Chen, F. Shen, Biocorrosion properties and blood and cell compatibility of pure iron as a biodegradable biomaterial, J. Mater. Sci. Mater. Med. 21 (2010) 2151–2163. [62] D. Zander, N.A. Zumdick, Influence of Ca and Zn on the microstructure and corrosion of biodegradable Mg–Ca–Zn alloys, Corro. Sci. 93 (2015) 222–233. [63] L. Chen, Y. Sheng, H. Zhou, Z. Li, X. Wang, W. Li, Influence of a MAO+ PLGA coating on biocorrosion and stress corrosion cracking behavior of a magnesium alloy in a physiological environment, Corros. Sci. 148 (2018) 134–143. [64] C. Shuai, B. Wang, Y. Yang, S. Peng, C. Gao, 3D honeycomb nanostructure-encapsulated magnesium alloys with superior corrosion resistance and mechanical properties, Comp. Part B. 162 (2019) 611–620. [65] F. Lyu, J. Gao, N. Sun, R. Liu, X. Sun, X. Cao, L. Wang, W. Sun, Utilisation of propyl gallate as a novel selective collector for diaspore flotation, Miner. Eng. 3 (2016) 32–43. [66] M. Erinc, W.H. Sillekens, R. Mannens, R.J. Werkhoven, Applicability of existing magnesium alloys as biomedical implant materials, Corro. Sci. 1 (2009) 209–214. [67] B. Liu, Y.F. Zheng, Effects of alloying elements (Mn, Co, Al, W, Sn, B, C and S) on biodegradability and in vitro biocompatibility of pure iron, Acta Biomater. 7 (2011) 1407–1420. [68] C. Shuai, S. Li, S. Peng, P. Feng, Y. Lai, C. Gao, Biodegradable metallic bone implants, Mater. Chem. Front. 3 (2019) 544–562.

Sci. Eng. B 4 (2018). [49] J. Lu, M. Descamps, J. Dejou, G. Koubi, P. Hardouin, J. Lemaitre, J.P. Proust, The biodegradation mechanism of calcium phosphate biomaterials in bone, J. Biom. Mater. Res. Part B. 63 (2010) 408–412. [50] Z. Xu, M. Hodgson, P. Cao, Effect of immersion in simulated body fluid on the mechanical properties and biocompatibility of sintered Fe–Mn-Based alloys, Metals 6 (2016) 309–318. [51] Z. Yin, M. Yan, Z. Bai, W. Zhao, W. Zhou, Galvanic corrosion associated with SM 80SS steel and Ni-based alloy G3 couples in NaCl solution, Electrochim. Acta 53 (2008) 6285–6292. [52] W. Sun, L. Wang, T. Wu, C. Dong, G. Liu, Tuning the functionalization degree of graphene: determining critical conditions for inhibiting the corrosion promotion activity of graphene/epoxy nanocomposite coatings, Mater. Lett. 240 (2019) 262–266. [53] L. Reclaru, R. Lerfb, P.Y. Eschlera, A. Blattera, J.M. Meyerc, Pitting, crevice and galvanic corrosion of REX stainless-steel/CoCr orthopedic implant material, Biomaterials 23 (2002) 3479–3485. [54] M. Wiemer, T. Butz, W. Schmidt, K.P. Schmitz, D. Horstkotte, C. Langer, Scanning electron microscopic analysis of different drug eluting stents after failed implantation: from nearly undamaged to major damaged polymers, Catheter. Cardiovasc. Interv. 75 (2010) 905–911. [55] Y. Yang, X. Guo, C. He, C. Gao, C. Shuai, Regulating degradation behavior by incorporating mesoporous silica for mg bone implants, ACS Biomater. Sci. Eng. 4 (2018) 1046–1054. [56] L. Lu, Y. Shen, X. Chen, L. Qian, K. Lu, Ultrahigh strength and high electrical conductivity in copper, Science 304 (2004) 422–426. [57] C. Shuai, P. Feng, P. Wu, Y. Liu, X. Liu, D. Lai, C. Gao, S. Peng, A combined nanostructure constructed by graphene and boron nitride nanotubes reinforces ceramic scaffolds, Chem. Eng. J. 313 (2017). [58] K. Kaviyarasu, N. Geetha, K. Kanimozhi, C.M. Magdalane, S. Sivaranjani, A. Ayeshamariam, J. Kennedy, M. Maaza, In vitro cytotoxicity effect and antibacterial performance of human lung epithelial cells A549 activity of zinc oxide doped TiO2 nanocrystals: investigation of bio-medical application by chemical

13