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PEG-based organic-inorganic hybrid coatings prepared by the sol-gel dip-coating process for biomedical applications.


The requirement of improving the quality of life of people affected by diseases which need replacements of tissues or body parts has encouraged the development of new materials with high performance in terms of tolerability and integration capability. Despite the advances in the biomaterials field, still today the average lifetime of an implant is about 20 years. This entails the need for subsequent replacement of the prosthetic device, especially in young patients.

Various classes of materials have been investigated to produce durable implants, such as metals, alloys, polymers, ceramics, and composites [1]. However, it is not currently possible to avoid the early failure of implants, because a good combination of properties (mechanical, chemical, and tribological) and biocompatibility of the materials has not been yet achieved.

In recent years, the surface modification of bio-inert metal implants with bioactive and biocompatible coatings is proving a promising strategy to obtain prosthetic devices in which the good mechanical properties of the metals are combined with the biological properties of the materials applied on their surface [2-6], The material's integration, indeed, is closely related to the properties of the surface where the interaction with the surrounding tissue occurs.

In the present work, three bioactive and biocompatible organic-inorganic hybrid nanocomposites, consisting of polyethylene glycol (PEG 400) embedded in Si[O.sub.2], Zr[O.sub.2], and Ti[O.sub.2] matricies, respectively, were used to prepare thin films in order to modify the surface of titanium grade 4 implants (material of choice in the orthopedic and dental fields) with the aim of improving the osseointegration ability of the substrate. The characterization of chemical structure and biological properties of Si[O.sub.2]/PEG and Zr[O.sub.2]/PEG hybrids, indeed, were already ascertained elsewhere [7-9], as a function of the polymer content. Moreover, taking into account the PEG ability of enhancing the biocompatibility of Si[O.sub.2] and Zr[O.sub.2] matrices and the biocompatibility of Ti[O.sub.2] (investigated previously [10]), the synthesis of new Ti[O.sub.2]/PEG hybrids was also proposed in this study and the ability of such three hybrid systems to transfer their biological activity to the bio-inert titanium substrates, when used as coating, was evaluated. Moreover, a comparison of the biological performances of the coatings obtained was carried out to assess the best composition to be used in the biomedical field.

The organic-inorganic hybrid nanocomposites were synthesized by means of the sol-gel technique, a method to produce glass and ceramics at low temperature. The process involves hydrolysis and condensation reactions of metal alkoxide precursors in a water-alcohol solution (sol), which lead to the formation of a 3D network (gel) [11]. The chemistry of the sol-gel technique leads to the formation of -OH groups on the material surface which makes the sol-gel materials more bioactive than those with the same composition but obtained with different techniques [12, 13]. Moreover, the low processing temperature makes the sol-gel method ideal for the production of organicinorganic hybrid nanocomposites by entrapping organic thermally labile compounds into a glassy matrix. These materials are considered as biphasic materials, where the organic and inorganic phases are mixed on the nanometer scale. Their properties derive from a synergistic effect between the individual constituents of the hybrid. Therefore, the guiding idea in the development of an organic-inorganic hybrid material is to overcome the drawbacks and to retain the best properties of each hybrid component [14].

The sol-gel method is easily coupled with several coating techniques, such as spray coating, spin coating, or dip coating [15]. The latter is a versatile and cheap method which allows thin films to be obtained by the dipping and withdrawal of a substrate from a sol with a controlled and constant speed. The withdrawal speed is a very important parameter, as it influences the thickness and the morphology of the obtained coatings [11, 15, 16]. Therefore, a sol-gel dip coating route was used to apply the bioactive and biocompatible hybrid coatings on titanium grade 4 substrates. The chemical structure and morphology of the coatings were investigated by attenuated total reflectance Fourier transform infrared (ATR-FTIR) spectroscopy and scanning electron microscopy (SEM). Moreover, to evaluate improvements in the biological properties of coated substrates, a comparative study was carried out in order to assess the samples' bioactivity and cytotoxicity in vitro as a function of the used matrix and PEG content. The results were compared with those obtained for uncoated titanium.


Sol-Gel Synthesis

The organic-inorganic hybrid materials with 6, 12, 24, and 50 wt% PEG were prepared at room temperature under atmospheric pressure. Silica-based materials were synthesized using tetraethyl orthosilicate (TEOS, Si[(O[C.sub.2] [H.sub.5]).sub.4], Sigma-Aldrich) as precursor of the inorganic phase. It was added dropwise to a solution containing ethanol (99.8%, Sigma-Aldrich), distilled water, and nitric acid (HN[O.sub.3] [greater than or equal to]65%, Sigma-Aldrich), used as a catalyst. The mixture was stirred for 15 min. Another solution was prepared by mixing polyethylene glycol (PEG 400, SigmaAldrich) with ethanol. This was added to the first mixture. The sol was stirred for 1 h at room temperature and then kept at room temperature away from dust. The solution obtained had a mole ratio of TEOS:HN[O.sub.3]:EtOH:[H.sub.2]O of 1:1.7:6:2 [7],

The hybrid organic-inorganic Zr[O.sub.2]-based materials were prepared from analytical reagent grade zirconium propoxide, Zr[(O[C.sub.3][H.sub.7]).sub.4] (Sigma-Aldrich) in ethanol, distilled water, and acetylacetone (AcAc, Sigma-Aldrich). This was added to control the hydrolytic activity of zirconium alkoxide. The solution obtained had a mole ratio of Zr[(O[C.sub.3][H.sub.7]).sub.4]:[H.sub.2]O:AcAc:EtOH of 1:1:4,5:6. PEG 400, dissolved in ethanol, was added dropwise to the solution under vigorous stirring. After the addition of reactant, the solution was stirred up to the point where homogeneous and transparent sols are obtained [9],

The organic-inorganic Ti[O.sub.2]-based materials were prepared using titanium butoxide (TBT), as a precursor of the inorganic matrix. A titanium(IV) butoxide solution (Ti[(O[C.sub.4][H.sub.9]).sub.4], 80 wt% in n-butanol, Sigma-Aldrich) was added to a mixture of n-butanol (BuOH), distilled water and glacial acetic acid (HAc) using the molar ratio TBT:Bu0H:HAc:[H.sub.2]O of 1:7,5:1,5:2 |10]. The reagent HAc was used to decrease the hydrolytic activity of titanium alkoxide because it acts as a chelating agent. Also in this case, PEG was added after previous dissolution in ethanol.

The solutions of PEG in ethanol used to synthesize the hybrid systems had different polymer concentrations (0, 6, 12, 24, 50 wt%), so that five hybrid materials for each matrix were obtained.

Coating Procedure and Characterization

The hybrid sols, 24 h after synthesis, were used to coat titanium grade 4 disks (Ti-gr4, Sweden & Martina, Padua, Italy) of 8 mm diameter and 2 mm thickness, using a dip-coater (KSV LM. Stockholm, Sweden). The disks were provided with a pin to facilitate the connection with the apparatus clamp (Fig. 1).

The substrates were cleaned with acetone in an ultrasonic bath for 30 min; subsequently the disks were subjected to a passivation process with HN[O.sub.3] (65%, Sigma-Aldrich) for 60 min. In order to assess the most opportune times for dip coating and withdrawal speeds, some preliminary tests were performed. For each sol, several speeds and times were tested and the obtained coatings were observed by SEM. The procedures which gave the best results in terms of cracks and coating homogeneity were adopted to prepare the final coatings for the other analyses. The sols were used for the coating procedure 24 h after the synthesis and the withdrawal speeds were set to 25 mm/min for silica and titania and 35 mm/min for zirconia. The thickness and the morphology of the obtained films are because of a combination of factors. The viscosity of the sol also plays an important role: for a given delay after synthesis, the viscosity changes as a function of alkoxide precursor reactivity. Since the thickness depends on both viscosity and withdrawal speed (according to Landau and Levich [16]), the use of different withdrawal speeds were required to obtain layers with a consistent thickness and morphology.

The coated substrates were heat-treated at 45[degrees]C for 24 h to promote film densification without any polymer degradation. Figure 2 shows the flow-chart of hybrid synthesis and of the coating procedure. The residue sols were left to gel at room temperature.

To analyze the chemical composition of the obtained coatings and the interactions between the organic and inorganic component within the hybrid materials, attenuated total reflectance Fourier transform infrared (ATR-FTIR) spectra were recorded on a Prestige-21 FT1R spectrometer equipped with an A1M-8800 infrared microscope (Shimadzu, Japan), using the incorporated 3-mm diameter Ge ATR semicircular prism. The spectra were recorded using a 30[degrees] angle of incidence for a total of 50 scans at a resolution of 4 [cm.sup.-1] over the range 650-4,000 [cm.sup.-1]. The spectra were analyzed by Prestige software (IR solution).

The morphology of the obtained coatings was observed using a scanning electron microscope (SEM, Quanta 200, FEI Europe Company, Netherlands). Coated substrates were fixed on aluminium stubs with colloidal graphite.

Bioactivity Characterization

The coated substrates were immersed in SBF (simulated body fluid) to evaluate their bioactivity at 37[degrees]C for 21 days. SBF is an acellular aqueous solution with an inorganic ion composition almost equal to that of human plasma. It was prepared by dissolving NaCl, NaHC[O.sub.3], KCl, [MgCl.sub.2]6[H.sub.2]O, [CaCl.sub.2], [Na.sub.2]HP[O.sub.4], [Na.sub.2]S[O.sub.4] (Sigma-Aldrich) in ultra-pure water and buffered at physiological pH 7.40 using 4-(2-hydroxyethyl)piperazine-l-ethanesulfonic acid hemisodium salt (HEPES, Sigma-Aldrich) and NaOH. As the formation of the hydroxyapatite layer is influenced by the ratio of the total exposed sample surface to SBF volume, that ratio was kept constant as reported in the literature [17], After 21 days, the materials were gently washed in distilled water and left in a desiccator for 24 h. The hydroxyapatite layer was examined with SEM Quanta 200 equipped with Electron Dispersion Spectroscopy (EDS).

Biological Property Characterization

The hybrids' biocompatibility was assessed by growing NIH 3T3 murine fibroblasts (ATCC, VA, USA) on coated and uncoated surfaces and their viability was examined via the WST-8 Assay (Dojindo Molecular Technologies Inc., MD, USA).

Cells were amplified in DMEM medium (Gibco, CA, USA) with 10% (v/v) foetal bovine serum, 1% pen-strep, in a humidified incubator, at 37[degrees]C, 5% C[O.sub.2], and 95% air.

Ti-gr4 disks were placed on the bottom of a 24-well plate, using three coated disks for each system (0, 6, 12, 24, and 50 wt% of PEG) and uncoated disks for the negative control. Disks were sterilized using a UV lamp.

The cells grown on the well bottom have been considered to represent 100%. viability; each point was performed in triplicate.

NIH 3T3 cells were amplified in a 25 [cm.sup.2] flask and at semiconfluence were detached using trypsin-EDTA (Gibco) composed of 2.5% w/v of trypsin and 0.2% w/v EDTA in phosphate buffered saline (PBS). About 5,000 cells were seeded on Ti-gr4 disks as well as on the well bottom. After 24 h of incubation, they were washed three times with PBS and were again incubated with 10% v/v of WST-8 in a fresh medium (50 ml in 500 ml of culture medium) for 2 h.

The tetrazolium salt of WST-8 [2-(2-methoxy-4-nitrophenyl) -3-(4-nitrophenyl)-5-(2,4-disulfophenyl)-2H-tetrazolium, monosodium salt] was used as a metabolism indicator, as that salt penetrates into the viable cells, where it is metabolized in the mitochondria. Tetrazolium is a water-soluble salt of purple color that dehydrogenases convert into yellow-orange crystals of formazan. The amount of formazan is directly proportional to the number of viable cells. The quantitative evaluation was performed by a spectrophotometer (Biomate 3, Thermo Scientific), measuring the UV absorbance at 450 nm.


Chemical Characterization and Coating Morphology

Previous work reports the chemical characterization of Si[O.sub.2]/ PEG and Zr[O.sub.2]/PEG gels with the same composition as the coatings investigated here [7-9]. NMR and FTIR analyses proved that in all hybrid nanocomposites the organic and inorganic components interact by means of H-bonds formed between ether oxygen and/or terminal -OH groups in PEG chains and the -OH groups of the inorganic matrices.

In the present work, the chemical structure of the coatings was ascertained by means of ATR-FTIR spectroscopy.

Figures 3 and 5 show ATR-FTIR spectra of the PEG-based hybrid materials (curves from b to e) compared to PEG-free Si[O.sub.2], Zr[O.sub.2], and Ti[O.sub.2] inorganic matrices (curve a) and pure PEG (curve f). In the spectra of all the hybrid materials the peaks typical of each inorganic matrix are visible [9, 10, 18, 19], However, the intensity of the peaks decreases with an increase in the polymer amount, regardless of the matrix, confirming that new interactions occur between the organic and inorganic components in each hybrid coating. In the spectra of the hybrid coatings some peaks related to PEG [20] are also visible which vary as a function of the matrix and polymer concentration.

In the FTIR spectra of the Si[O.sub.2] + PEG hybrid coatings (Fig. 3), PEG peaks appear only when 24 wt% of polymer was added. In particular, the signals because of C-H stretching and bending vibrations, at 2,920, 1,454, and 1,354 [cm.sup.-1], and to C-O at 1,296 [cm.sup.-1] are visible. Their intensity increases when 50 wt% was incorporated. Moreover, a peak at 1,735 [cm.sup.-1], absent in both pure Si[O.sub.2] and PEG spectra, is visible, which suggests that an oxidation of PEG and the formation of a product containing a C=O group occurred. The PEG degradation arises only when it is embedded in the Si[O.sub.2] matrix, as HN[O.sub.3] used in the synthesis process induces the oxidation reaction [20, 21].

In the spectra of Zr[O.sub.2] + PEG hybrid coatings (Fig. 4), some PEG peaks are already visible in the system containing 6 wt% PEG (curve b). In particular, the peak at 2,900 [cm.sup.-1] is because of C-H stretching and the peak at 1,100 [cm.sup.-1] is ascribable to C-O-C vibrations. Moreover, the intensity of the weak peak, visible in the Zr[O.sub.2] spectrum (curve a) at 940 [cm.sup.-1] and because of C-C in AcAc, grows with the PEG content, as the vibrations of C-C bonds in the polymer chains also contribute to its intensity. In the spectra of the Zr[O.sub.2]-based hybrids containing higher PEG amounts, the intensity of its peaks increases and other bands ascribable to the polymer appear. In the spectra of Zr[O.sub.2] + 12 wt% PEG hybrid (curve c) the peaks of C-OH and the vibrations of C-C bonds in the polymer chains appear at 1,250 [cm.sup.-1] and in the range 800-900 [cm.sup.-1]. Moreover, in the spectra of Zr[O.sub.2] + 24 wt% PEG hybrid (curve d) the peak related to C-H bending at 1,450 [cm.sup.-1] is also visible. When 50 wt % of polymer was added, the spectrum (curve e) is dominated by PEG signals and other two weak peaks are observed at 1,290 and 1,350 [cm.sup.-1] because of C-H scissoring vibrations.

In the spectra of Ti[O.sub.2] + PEG hybrids (Fig. 5) signals of the polymer are already visible in the system containing 6 wt% PEG (curve b). This spectrum also shows the peaks attributed to C-H and C-O-C stretching at 2,900 and 1,100 [cm.sup.-1]. In the spectrum of Ti[O.sub.2] + 12 wt% PEG. the intensity of those peaks increases and the peak because of C-OH vibrations appears at 1,253 [cm.sup.-1]. The intensity of all peaks increases with PEG content and when 50 wt% of polymer was included the PEG signals dominate the spectrum (curve e). Moreover, the signals related to C-H scissoring at 1,442 and 1,296 [cm.sup.-1] appear. In the spectra of Zr[O.sub.2] + PEG hybrids (Fig. 4), there is no evidence of interaction between the inhibitor AcAc and the polymer, whereas in the spectra of Ti[O.sub.2] + PEG hybrids (Fig. 4), an increase in the C = O peak intensity at 1,710 [cm.sup.-1] was observed with increasing PEG amounts. This suggests an interaction between the inhibitor acetic acid and the polymer.

Microstructural analysis of the coatings was carried out by SEM microscopy. The coated substrates were observed after heat treatment and the thin film micrographs are shown in Fig. 6. In all images curved marks are observed because of the metal-turning of the disks. The PEG-free coatings show fractures (evident in the left column of Fig. 6) which disappear gradually at increasing polymer percentages (data not show). The right column of Fig. 6 shows silica-, zirconia-, and titaniabased coatings with 50 wt% of PEG without fracture. These data suggest that the addition of high amounts of polymer causes an increase of sol viscosity which leads to a more uniform deposition of the layers using the dip-coating process. In contrast, since the PEG-free sols are less viscous, a less uniform deposition results and crack formation occurs. The presence of PEG can also increase both the coating elasticity which is reflected in a decrease in the coating fractures. Moreover, all the layers appear homogeneous and no phase separation is detected at high magnification. In these coatings the organic and inorganic phases interpenetrate on a scale of less than 1 pm, proving that the layers consist of hybrid materials according to IUPAC definition [22],

Biological Properties Results

The SEM micrographs of the samples recorded after soaking in SBF show evidence of the formation of globules on the sample surface. The globular morphology of this precipitate is typical of the bone-like apatite which nucleates on bioactive materials when they are soaked in SBF solution, as widely reported in the literature [17]. After 21 days, the whole surface of all coated samples is covered by this globular precipitate (Fig. 4). Its typical shape and EDX analyses identify it as hydroxyapatite. An atomic content ratio Ca/P < 1.67 (in the range 1.56-1.62) has been recorded for all samples. This result suggests that the precipitate does not consist of stoichiometric hydroxyapatite but of Ca-deficient type apatite [23]. The apatite formed in SBF is, indeed, similar to bone apatite because it is generally a Ca-deficient type apatite with lower Ca/P atomic ratio than stoichiometric one (ISO 23317:2014). Materials able to induce hydroxyapatite nucleation when soaked in SBF will potentially be able to bond the living bone when implanted in vivo by the formation of a bone-like apatite layer on their surface. Therefore, this in vitro test is widely used in the biomaterials field in order to predict the osseointegration ability of new materials in vivo. The PEG percentage in coatings does not cause any appreciable difference in terms of hydroxyl apatite nucleation on coated surfaces. For this reason, Fig. 7 shows only a single micrograph for each system.

Figure 8 shows the viability values of the cells grown on coatings of silica, titania, and zirconia-based systems wilh 0, 6. 12, 24, and 50 wt% PEG on uncoated Ti-gr4. The viability of cells seeded on coated disks improves compared to that of the cells seeded on polystyrene (considered 100% of vitality) and uncoated titanium. The inorganic matrix affects biological properties. The best cell response, indeed, was detected with Si[O.sub.2] coatings and, thus, with the Si[O.sub.2]-based hybrid coatings. However, all the hybrid coatings prove more biocompatible than inorganic ones. This means that PEG improves the films biocompatibility probably by two mechanisms: first acting as plasticizer and, thus, allowing crack-free coatings to be obtained [24. 25]; second, inducing a surface hydrophilicity increase which favors protein adhesion [26].


Hybrid materials based on silica, zirconia, and titania with different PEG percentages were synthesized with the sol-gel technique and used to coat titaniun grade 4 disks substrates by means of a dip coating procedure. A comparative study demonstrated that polymer amount in the hybrids affects the film morphology and biocompatibility. In particular, a high PEG content decreases the formation of cracks and improves the biocompatibility of the obtained coatings. The matrix also influences biocompatibility. Higher cell proliferation was found in response to Si[O.sub.2]-based coatings. On the other hand, all hybrids were shown to be bioactive (regardless of matrix and PEG content), a fundamental property for their osseointegration after implantation.


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Michelina Catauro, Ferdinando Papale, Giusi Piccirillo, Flavia Bollino

Dipartimento di Ingegneria Industriale e dell'lnformazione, Seconda Universita di Napoli, Via Roma 29, Aversa, CE, 81031, Italy

Correspondence to: M. Calauro; e-mail: (For the synthesis of the hybrid materials and coating preparation) and F. Bollino; e-mail: (For sample characterization)

DOI 10.1002/pen.24488

Published online in Wiley Online Library (

Caption: FIG. 1. Dip Coaler apparatus and enlarged view of the titanium grade 4 substrates (in the box).

Caption: FIG. 2. Flow chart of materials synthesis und coating procedure. The molar ratios among the reagents are reported.

Caption: FIG. 3. ATR-FTIR spectra of (A) Si[O.sub.2], (B) Si[O.sub.2] + 6 wt% PEG; (C) Si[O.sub.2] + 12 wt% PEG. and (D) Si[O.sub.2] + 24 wt% PEG; Si[O.sub.2] + 50 wt% PEG coalings.

Caption: FIG. 4. ATR-FTIR spectra of: (A) Zr[O.sub.2], (B) Zr[O.sub.2] + 6 wt% PEG; (C) Zr[O.sub.2] + 12 wt% PEG, and (D) Zr[O.sub.2] + 24 wt% PEG; Zr[O.sub.2] + 50 wl% PEG coatings.

Caption: FIG. 5. ATR-FTIR spectra of: (A) Ti[O.sub.2], (B) Ti[O.sub.2] + 6 wt% PEG; (C) Ti[O.sub.2] + 12 wt% PEG, and (D) Ti[O.sub.2] + 24 wt% PEG; Ti[O.sub.2] + 50 wt% PEG coatings.

Caption: FIG. 6. SEM micrographs of coatings without polymer (left column), with 50 wt% PEG (right column).

Caption: FIG. 7. Hydroxyapatite layer on the surface of a sample after 21 days and EDS analysis. [Color figure can be viewed at]

Caption: FIG. 8. Results of cell viability on silica, zirconia, and titania coatings and uncoaled titanium (Ti); cells grown on polystyrene were considered 100%.
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Author:Catauro, Michelina; Papale, Ferdinando; Piccirillo, Giusi; Bollino, Flavia
Publication:Polymer Engineering and Science
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Date:Jun 1, 2017
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