Journal of Materials Science

, Volume 52, Issue 15, pp 9082–9090 | Cite as

Engineering the surface functionality of 45S5 bioactive glass-based scaffolds by the heterogeneous nucleation and growth of silver particles

  • Thomas Meincke
  • Valentina Miguez Pacheco
  • Daniel Hoffmann
  • Aldo R. Boccaccini
  • Robin N. Klupp Taylor
In Honor of Larry Hench

Abstract

An emerging topic in the field of biomaterials is the incorporation of silver ions, metallic silver or silver oxides into bioactive glasses to impart novel functionalities. In this work, a new approach of surface functionalization of 45S5 bioactive glass (BG) is introduced. In contrast to more common methods, which are based on the inclusion of silver during the sol–gel synthesis of BG, our method allows the surface functionalization of BG powders and BG scaffolds after their preparation. Hereby, we demonstrate the transferability of a previously reported approach on the wet chemical synthesis of cup-like and dendritic silver patches first from colloidal silica particles to BG particles and further to macroscopic highly porous BG scaffolds which were prepared by the sacrificial foam replica technique. The time-dependent silver releases of BG scaffolds with different silver loadings into simulated body fluid (SBF) were measured. Further studies were addressed to investigate the bioactivity of BG scaffolds before and after the silver coating procedure. It was found the silver deposition on 3D BG scaffolds did not affect the formation of crystalline hydroxyapatite during immersion into simulated body fluid.

Introduction

Since L.L. Hench found in 1969 that a silicate glass composition (known as 45S5 Bioglass®) could bond strongly to bone [1], the field of BGs has been expended continuously and different types of glass substrates like BG powders [2, 3, 4], BG pellets [5, 6, 7] and macroscopic highly porous scaffolds [8, 9, 10, 11, 12] have been developed. BGs are characterized by their bioactivity, meaning the formation of crystalline hydroxyapatite (HA) on the surface of BG substrates when immersed into relevant physiological fluid like simulated body fluid (SBF), which makes BGs highly interesting biomaterials for bone regeneration [13, 14]. A current main focus in research is to include further functionalities into BG by incorporating biologically active ions [15], for example, lithium for cell stimulation in bone formation [16] or silver [17, 18, 19, 20, 21, 22, 23] and copper [24, 25, 26] for antibacterial activity. While in most cases silver-doped BGs get derived by the sol–gel method under the addition of a further silver salt like silver nitrate [17, 27, 28, 29], for non-bioactive antimicrobial substrates like glass or polymer fibers, also methods which are based on the immobilization of silver nanoparticles at their surface are reported [30, 31]. In contrast to these strategies, in the present work a new approach of surface functionalization of 45S5 BG-based scaffolds by heterogeneous nucleation of silver particles at the BG scaffolds surface is introduced. The process is based on the colloidal one-pot synthesis of silver patchy particles onto Stöber silica particles [32], as established in batch [33] and continuous-flow synthesis [34] by Klupp Taylor and co-workers. Within both approaches, colloidal silica particles (dp < 500 nm) were dispersed in silver nitrate and formaldehyde solution. By subsequent addition of diluted ammonia hydroxide solution, the reduction reaction between silver and formaldehyde was initiated, leading to heterogeneous nucleation and surface conformal growth of dendritic and cup-like silver patches.

The present work is addressed to demonstrate the transferability of this silver patch synthesis optimized for colloidal particles to BG particles and further on macroscopic highly porous substrates like highly porous 3D BG scaffolds via immersion technique, as illustrated in Fig. 1. The effect of a change in process parameters like silver nitrate concentration and the number of silver coating steps on the amount of deposited silver and the consequently released silver ion concentration in simulated body fluid (SBF) were of interest. Hence, the influence of the silver coating process on the bioactivity of the BG scaffolds was investigated.
Figure 1

Experimental setup for silver coatings of 45S5 bioactive glass scaffolds

Materials and methods

Preparation of bioactive glass scaffolds

BG scaffolds were prepared by the foam replica technique as established by Chen et al. [8]. Briefly, BG powder of 45S5 composition from Schott AG was grinded using a Retsch (PM 100) zirconia ball planetary mill to adjust the median glass particle size to below 5 µm. 15.66 g of the derived powder was dispersed into a slurry containing 1.1 g polyvinyl alcohol (PVA) and 25 mL Millipore water and stirred for 30 min at 80 °C. After the slurry was allowed to cool down to room temperature, cubic 10 mm × 10 mm 45 ppi polyurethane (PU) foams (Eurofoam) were immersed into the slurry for 1 min. Afterward the excessive slurry was squeezed out of the foams. This whole procedure was repeated once to increase the loading of BG particles on the foams surface. The as-prepared soaked foams were dried overnight at 60 °C before being sintered in a high-temperature (Nabertherm P330) furnace. The temperature profile is shown in Fig. S1.

Silver coatings on bioactive glass powder

45S5 BG powder was coated by silver particles according to the method reported by Bao et al. [33] with minor changes in concentrations and core particles. Briefly, a suspension of 5.7 mg BG powder and 5 mL of silver nitrate at concentrations between 30 and 90 µM (see main text for details) was heated to 50 °C. Afterward, 30 µL of 37% formaldehyde solution was added. To initiate the silver reduction reaction, a total volume of 30 µL of 8% ammonia solution was added dropwise within 30 s under vigorous stirring.

Silver coatings on bioactive glass scaffolds via immersion technique

For the synthesis of silver patches on BG scaffolds, the volumes of all solutions used in the reaction described in "Silver coatings on bioactive glass powder" section were doubled. The BG scaffold, which was fixed with tweezers, was immersed into the silver nitrate solution while leaving a sufficient gap below it for vigorous stirring at 50 °C, as illustrated in Fig. 1. Following this, 60 µL of formaldehyde was added and subsequently 60 µL of 8% ammonia solution was added dropwise within 30 s under vigorous stirring. For samples which were multiply treated, the same procedure was applied up to five times, all solutions being freshly prepared for each silver coating step with a silver nitrate concentration of 90 µM.

Bioactivity and silver release of bioactive glass scaffolds

The formation of hydroxyapatite (HA) and the release of silver ions were investigated in simulated body fluid (SBF) which was prepared based on the work of Kokubo et al. [35]. For the examination of the bioactivity and the silver release, a set of five BG scaffolds was prepared at the same conditions of the silver coating procedure. Each of these BG scaffolds was cut into four pieces of similar mass. Three of these pieces were immersed together into ~50 mL SBF by adjusting the mass concentration to 1.5 mg/mL and placed in an orbital shaker (KS 4000i control, IKA®) for up to 30 days at 37 °C. After different times, the precipitation of HA on the BG scaffolds was examined by FTIR, XRD and SEM image analysis. In addition, the silver release into the SBF supernatant above the BG scaffolds was investigated by inductively coupled plasma-optical emission spectroscope (ICP-OES).

Characterization

For the investigation of the morphology and elemental composition of BG powder and BG scaffolds after silver particles synthesis, scanning electron microscopy (SEM) and energy-dispersive X-ray spectroscopy (EDX) analyses were performed using an Auriga FIB-SEM Instrument (Zeiss, Germany). For X-ray diffraction measurements (XRD) before and after the precipitation of HA on BG, a D8 Advance (Bruker AXS, Germany) device in Bragg–Brentano geometry with a Cu Kα radiation source (λ = 0.154058 nm) was used. XRD patterns in the 2θ range of 10°–70° were recorded. For Fourier transform infrared spectroscopic measurements (FTIR) with a Nicolet 6700 FTIR spectrophotometer (Thermo Scientific USA), KBr pellets with 1 wt% of crumbled BG scaffolds were prepared. The silver content in SBF was measured by using Perkin Elmer Optima 8300 inductively coupled plasma-optical emission spectroscope (ICP-OES).

Results and discussion

Patchy silver coating on bioactive glass powder

Before the actual silver coating experiments with the BG scaffolds were carried out, first test reactions were processed with BG powder. The reaction conditions chosen have been already known from previous published work of Bao et al. [33] and further preliminary experiments to form dendritic silver patches. Figure 2a–c shows the suspensions of BG powder after the silver coating synthesis. It can clearly be seen that with increasing silver nitrate concentration the color of the suspension becomes darker indicating an increase in the absolute amount of deposited silver. Since a synthesis without the presence of BG powder leads to a brownish to orange suspension of free silver particles (data not shown), we conclude that all the silver nucleated and grew on the BG particles. The silver deposition after a synthesis with 90 µM silver nitrate concentration can be seen on the SEM images in Fig. 2d, e, g. By EDX analysis, the presence of silver at the BG powder surface could be confirmed, as demonstrated in Fig. 2f. Interestingly, the deposition of silver does not show a surface conformal or dendritic structure as was seen in earlier work using colloidal silica particles [33]. A potential reason for this could be the additional components (beyond silica) of BG of 45S5 composition, interfering with the mechanism of metal conformal growth.
Figure 2

ac BG powder suspension after silver coating synthesis at 30, 60 and 90 µM silver nitrate solution, d, e SEM images of same BG particle showing silver deposition at two different magnifications synthesized with 90 µM silver nitrate concentration, f EDX analysis of BG powder confirming the presence of silver after synthesis at 90 µM silver nitrate, g SEM image showing the position of EDX analysis

Patchy silver coating on bioactive glass scaffolds

Similar as presented for BG powder, the silver nitrate concentration for the silver coating on BG scaffolds was experimentally optimized within a first set of experiments at different silver nitrate concentrations ranging from 60 to 150 µM (shown in Fig. S2). It can be seen that after silver coating the BG scaffolds turned different shades of gray depending on the silver nitrate concentration. Interestingly, an increase in darkness of the scaffold was just observed with an increase in the silver nitrate concentration from 60 to 90 µM. The scaffolds treated by silver coating at higher silver nitrate concentrations of 120 and 150 µM showed a less intensive gray color, indicating a deposition of less silver. We assume the surface exposed by one scaffold and the overall undefined mixing conditions during the silver coating procedure lead to a higher nucleation rate and consequently to the occurrence of more homogeneous nucleation in the scaffold surrounding aqueous bulk phase. From this preliminary set of experiments, we conclude that a concentration of 90 µM silver nitrate leads to the optimum ratio of heterogeneous nucleation at the scaffolds surface to homogeneous nucleation in the bulk phase of silver particles.

Since the overall silver loading at the scaffolds’ surface which can be achieved within one step is limited, we decided to use the same scaffold for up to five iterations of the silver coating procedure to increase the final amount of silver deposited. Figure 3 shows SEM images of the surface of BG scaffolds before silver coating (Fig. 3a) and after up to five iterations of coating (Fig. 3b–f). It can be seen that after one coating step very small silver particles were deposited onto the BG scaffold—most probably by heterogeneous nucleation. With increasing number of coating steps, first the amount and later also the size of the deposited silver particles increased. The formation of silver was additionally confirmed by EDX analysis for the sample after five silver coatings (shown in Fig S3). Similar to the case for BG powder, regardless of the number of coating steps, no surface conformal patches were formed. Figure S4 shows corresponding photographs of the BG scaffolds indicating a trend to darker colors with increasing silver loading.
Figure 3

a Plain 45S5 BG scaffold, bf 45S5 BG scaffolds after increasing number of silver coating iterations

Silver release of bioactive glass scaffolds

After the synthesis of particulate silver coatings, the BG scaffolds were immersed up to 30 days into simulated body fluid (SBF). Figure 4 shows the time-dependent silver release of the silver-coated BG scaffolds with different silver loadings. In the case of scaffolds which were coated just once by silver, the silver release was still below the limits of ICP-OES measurements after 3 days of immersion into SBF. For longer immersion times from 14 to 30 days, an increasing silver release from ~0.1 to ~0.25 mg/mL could be observed. For scaffolds which were treated by silver reduction reaction three and five times, a silver release of ~0.1 mg/mL after 24 h with an increasing trend up to ~1.2 and ~1.9 mg/mL, respectively, was measured. However, the comparison of the silver release after 14 and 30 days shows a trend to higher values with an increasing number of silver coating steps.
Figure 4

Time-dependent silver release of BG scaffolds immersed into SBF determined by ICP-OES measurements

Bioactivity of bioactive glass scaffolds

The bioactivity of the BG scaffolds was examined with and without the deposition of silver on the surface. SEM images of the BG scaffolds were taken after three, five and 14 days of immersion into SBF, as illustrated in Fig. 5a–c. It can be seen that after three days, first cauliflower-like structures were formed on the BG scaffold surface, as is typical for the formation of hydroxyapatite [12, 36, 37]. As expected, the amount and size of these structures increased over the course of 14 days. Figure 5d shows the corresponding FTIR spectra for a plain and a five-time silver-coated BG scaffold before and after the immersion into SBF for 14 days. All spectra show the typical Si–O–Si absorption bands between 1000 and 1100 cm−1 and a peak for \( {\text{PO}}_{4}^{3 - } \) at 1035 cm−1. Before the immersion into SBF, both the spectra of the plain and the five-time silver-coated BG scaffolds show a strong and broad absorption band from 900 and 960 cm−1 which can be associated with the Si–O non-bridging oxygen (NBO) absorption bands [38] and peaks for apatite-like phases around 620, 575 and 530 cm−1, while the non-splitting peak around at 575 cm−1 for P–O bending indicates a non-crystalline unstable calcium phosphate phase [39]. In addition, the spectra of the plain scaffold before immersion into SBF show a clear shoulder at 840 cm−1 for Si–O–2NBO [38] groups which gets less significant after five silver coating steps. Together with additional very weak absorption bands between 3200 and 3600 cm−1 for Si–OH groups [40, 41, 42] (see Fig. S5), apparently before the immersion of the BG scaffold into SBF, siloxane and phosphate groups govern the surface chemistry. We believe that the latter may hinder the surface conformal diffusion limited growth of silver patches. After 14 days of immersion into SBF, the Si–O–NBO and Si–O–2NBO absorption bands disappeared and the peak for \( {\text{PO}}_{4}^{3 - } \) at 1035 cm−1 becomes more defined. In addition, absorption bands for \( {\text{CO}}_{3}^{ - 2} \) vibrations at 1460 ccm−1 and vibrational bands in tetrahedral \( {\text{PO}}_{4}^{3 - } \) at 565 and 602 cm−1 for P–O bending show up after immersion into SBF and are indicative for the formation of crystalline calcium phosphate [16, 43, 44]. Taken together, independent of the silver coating reactions, the bioactivity of the prepared BG scaffolds could be shown. For all samples discussed, corresponding XRD data are given in electronic supplementary material and in Fig. S6. Those data show only peaks corresponding to the BG or hydroxyapatite. Crystalline silver was not detected due to the low amount present in comparison with the other crystalline materials. Indeed, a previous study of metal coating on BG did not detect low loadings of metal using XRD [45]. Finally, the sharp peaks in the XRD spectrum for the five-time silver-coated BG scaffold that had been aged in SBF for 14 days suggest a possible acceleration of the nucleation and growth of highly crystalline hydroxyapatite driven by the presence of silver nanoparticles on the surface [46]. This effect will be investigated in follow-up work.
Figure 5

ac SEM images of five-time silver-coated BG scaffold after being immersed into SBF for three to 14 days d FTIR spectra of plain and five-time silver-coated BG scaffolds before and after 14-day immersion into SBF. All spectra normalized to 1 at maximum between 1000 and 1100 cm−1

Conclusion

Within this work, it could be shown that a simple technique using the principle of heterogeneous nucleation of silver particles on a silica-related surface can be transferred from a colloidal synthesis using silica particles to BG powder and further to the coating of macroscopic highly porous structures like 3D 45S5 BG scaffolds. The FTIR analysis before silver coating of a plain 45S5 BG scaffold gave an insight into the present surface chemistry which is governed by siloxane and calcium phosphate groups. We believe, in contrast to our earlier work with colloidal silica particles, whose surface is governed by hydroxyl groups [47], the presence of different surface groups on 45S5 BG results in no surface conformal silver patch growth. However, by iteration of the silver coating procedure the amount of deposited silver could be increased. This allowed the tailoring of the absolute and time-dependent silver release of BG scaffolds in simulated body fluid. By SEM, FTIR and XRD measurements, the independence of the bioactivity on the silver coating reaction could be demonstrated. Future work is addressed to the manipulation of the surface chemistry of the BG scaffolds and advanced process design to achieve surface conformal diffusion limited growth of dendritic silver patches. In addition, electrical conductivity measurements and cytocompatibility tests will be conducted.

Notes

Acknowledgements

The authors are grateful to Fabrizio-Zagros Sadafi for fruitful discussions and for financial support from the Cluster of Excellence “Engineering of Advanced Materials” which is funded by the German Research Foundation (DFG) within the framework of the German Federal and State Excellence Initiative. V. Miguez Pacheco and Aldo R. Boccaccini acknowledge the European Commission funding under the 7th Framework Programme (Marie Curie Initial Training Networks; Grant Number 289958, “Bioceramics for bone repair”).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10853_2017_877_MOESM1_ESM.docx (1.6 mb)
Supplementary material 1 (DOCX 1601 kb)

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Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Institute of Particle TechnologyFAU Erlangen-NürnbergErlangenGermany
  2. 2.Institute of BiomaterialsFAU Erlangen-NürnbergErlangenGermany
  3. 3.Interdisciplinary Center for Functional Particle SystemsFAU Erlangen-NürnbergErlangenGermany

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