Effect of Morphology on the <i>In Vitro</i> Bioactivity and Biocompatibility of Spray Pyrolyzed Bioactive Glass

Chuni, Tsion; Dachasa, Kena; Gochole, Fekadu; Hunde, Tadele; Bakare, Fetene Fufa

doi:https://doi.org/10.1155/2023/5858858

Advances in Materials Science and Engineering

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Abstract Introduction Materials and Methods Results and Discussion Conclusions Data Availability Conflicts of Interest Authors’ Contributions Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2023 | Article ID 5858858 | https://doi.org/10.1155/2023/5858858

Effect of Morphology on the In Vitro Bioactivity and Biocompatibility of Spray Pyrolyzed Bioactive Glass

Tsion Chuni,¹Kena Dachasa,¹Fekadu Gochole,¹Tadele Hunde,^1,2and Fetene Fufa Bakare^1,2

Academic Editor: Roger Narayan

Received01 Nov 2022

Revised14 Mar 2023

Accepted06 Apr 2023

Published13 Apr 2023

Abstract

Because of its fundamental characteristics, including bioactivity, biodegradability, and nontoxicity, bioactive glasses (BGs) become among the most impressive materials in the area of biomedical applications. It is primarily utilized in the applications of dermal fillers, orthopedic implants, and pharmaceutical delivery systems. Here in this study, simple and continuous methods were employed to produce hollow spherical bioactive glasses (HSBGs) microspheres. Using a spray pyrolysis method, solid and hollow spherical particles were successfully synthesized, and the particle formation mechanism was also discussed in detail. Surface and inner morphologies of synthesized bioactive glass (BG) powders were investigated using scanning electron microscopy (SEM) and transmission electron microscopy (TEM), respectively. BET was employed to measure the pore volume as well as specific surface area for pure BG and BG-derived-PEG powders; all values are below 0.05, demonstrating noticeable distinction among both forms of synthesized powders. Using energy dispersive spectroscopy (EDS), the constituent components of prepared samples were assessed. In addition, by immersing samples in simulated bodily fluid (SBF) for 12 hr, in vitro bioactivity was tested by SEM. The viability of cells for both BG specimens was evaluated at various extraction concentrations by MTT assay (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenylte-trazolium bromide) for 72 hr. Relying on the Ca/P ratio obtained from SEM-EDS, HSBGs possessed higher hydroxyapatite-forming capacity than solid bioactive glasses (SBGs). In addition, the cell viability of both specimens showed that at all extraction concentrations, they pass the standard biocompatibility levels. Therefore, the HSBGs have better biocompatibility and in vitro bioactivity; hence they are promising for future tissue-engineering development.

1. Introduction

Bioactive glasses (BGs) have gained attention during recent decades for use in dermal fillers, drug delivery, tooth implants, and bone tissue [1–3]. Particularly, for its superior properties such as bioactivity, biodegradability, osteoconductivity, and biocompatibility, which stimulate new tissue growth which is comparable to compositions within the major inorganic components of human bones [4–8]. Among these properties, bioactivity and biocompatibility have received special attention extensively to enhance the clinical demand for BG’s performance [9, 10].

Hence, number of parameters influence the bioactivity and biocompatibility of the BGs such as compositions [11], morphology [11, 12], and surface areas [13]. For example, bioactive glass which contains hollow structures improves several properties such as injectability, flowability, and drug delivery, which are the most significant in tissue engineering [14–17]. Moreover, particles with spherical morphology also improves the activities of bone tissue regeneration, reduces inflammatory reactions [18, 19], and optimizes drug release [20] than irregular shape particle.

Several research works were reported related to the effect of morphology on bioactivity. Liu et al. showed that spherical and hollow BGs can be synthesized with poly (acrylic acid) (PAA) as a template by a sol-gel method in which the bond forming ability of the BGs improved [21]. In addition, spherical bioactive glasses particles with hollow structures have been attracted, because of their superior properties such as higher specific surface area, lower density, good flowability, and large porosity [22]. Furthermore, bioactive glass, which contains hollow structures have higher characteristic in vitro bioactivity as compared to a solid structure, owing higher specific surface area which improves the area where fluids and materials interact one another [16]. In addition, the morphologies were directly influencing the biocompatibility of the bioactive glasses. Kuo et al. studied that spherical and smooth sphere particles synthesized using spray pyrolysis method result in greater cell viability than irregular and rough surface particles [23]. Silica-based BG particles containing hollow structures have better advantages on bioactivity and biocompatibility. Because of silica glass degrades slowly and has unpredictable long-term effects, silica-free phosphate-based BGs are emerging. Phosphate-based glasses (PBG) have long-lasting effect in physiological environment and can be modified and managed for their ion release [24]. Dopants like fluoride must be added to PBGs to improve the biological characteristics by generating fluorapatite (FAp). When moderate amounts of fluoride are added to osteoblast cell cultures, the development of osteoblast cells is stimulated; conversely, greater concentrations of fluoride decrease osteoblastic activity [24]. Thus, the preparation of hollow silica-based BGs can reduce all these concerns related to silica glasses and silica-free PBGs.

So far, several methods have been used for synthesizing BG nanoparticles, such as spray drying, sol-gel, and spray pyrolysis methods. Among these methods, the sol-gel approach remains the most popular because of its chemical versatility and low-temperature synthesis [25, 26]. However, the entire procedure involves batch production and takes two to three days. On contrary, the pros of spray pyrolysis (SP) are relatively inexpensive, quick processing, and continuous production [4, 27, 28].

Surface morphologies and inner morphologies of the bioactive glass can affect bioactivity and biocompatibility of BGs. In our previous studies, PEG was utilized as a pore-forming agent that could greatly altered the morphology and the structure of BG particles properties, as well as biodegradability and bioactivity [5]. However, little consideration has been given to hollow spherical BG particles and their effect on the bioactivity and biocompatibility of BGs. In this work, we study the impact of morphology on the bioactivity and biocompatibility (cell viability) of spray pyrolyzed BGs.

Finally, synthesized powders were examined for surface and inner morphologies, specific surface area, elemental composition, and cell viability using SEM, TEM, Brunauer-Emmett-Teller (BET) method, EDS, and MTT assay, respectively.

2. Materials and Methods

2.1. Powder Preparation

58S BG powders (Pure BG and PEG-derived BG powders) consists of CaO (36 mol %), P₂O₅ (4 mol %), and SiO₂ (60 mol %) were synthesized by SP. Initially, BG precursors without PEG were prepared using calcium nitrate tetrahydrate (CN, Ca(NO₃)₂·4H₂O, 98.5 wt %, Showa, Osaka, Japan), triethyl phosphate (TEP, (C₂H₅)₃PO₄, 99 wt %, Alfa Aesar, Haverhill, MA, USA), and tetraethyl orthosilicate (TEOS, Si(OC2H5) 4, 99.9 wt %, Showa, Osaka, Japan) were used as the sources for Ca, P, and Si, respectively. The solution was made by mixing 60.00 g of ethanol with 1.60 g of 0.5 M HCl, adding 37.49 g of tetraethyl orthosilicate (TEOS), 25.50 g of calcium nitrate tetrahydrate (CN), and 4.37 g of triethyl phosphate (TEP). The PEG-derived BG particles were synthesized by adding additional 0.5 M, polyethylene glycol (PEG, 95.0 wt %, molecular weight of 600 g/mol, Showa, Tokyo, Japan). The final precursor solution was made by stirring it for 24 hours at room temperature [5]. For the SP procedure, a 1.65 GHz ultrasonic nebulizer (King Ultrasonic Co., Taiwan) was used to disperse the precursor solution into tiny droplets. In a tube furnace (D110, Dengyng, Taiwan), the droplets experienced thermal treatments that included preheating, calcining, and cooling at temperatures of 250°C, 550°C, and 350°C, respectively. High-voltage electrons generated from tungsten corona wire charged the particles’ surfaces (16 kV). After being neutralized, the negatively charged particles were condensed in an earthed stainless steel collector [29].

2.2. Characterization

For TGA analysis (TGA, Perkin-Elmer Model TGA-7), the precursor were placed under nitrogen flow to examine the decomposition temperature, in which the heating rate was 20 ^OC/min. In addition, surface and internal morphologies were examined by SEM (JSM-6500F, JEOL, Tokyo, Japan) and TEM (Tecnai G2 F20, FEI, Hillsboro, OR, USA), respectively. In order to ensure enough contrast, pictures were obtained at 15 kV while the powders were dispersed onto the SEM holders using conductive carbon tapes.

Particles were dispersed in acetone using an ultrasonicator for around 5 minutes to create powders for TEM analysis. A drop of the suspension was then applied to grids made of the holey carbon film. At normal temperatures, the solvent on the carbon grids evaporated. EDS (X-Max 50 mm2, Oxford Instruments, High Wycombe, UK), were used for compositional analysis. Furthermore, according to Kokubo’s procedure, simulated bodily fluid (SBF) that contains a similar ionic concentration with human plasma was employed for the study of bioactivity [30]. Then, the BG powders were poured in SBF solution followed by shaking in a thermostatic orbital shaker at 37°C for 24 hours while maintaining a pH of 7.4. The powders that were synthesized were dried for 24 hours at 70°C in an oven after being rinsed three times with deionized water and acetone. Finally, SEM was used to evaluate each specimen’s bioactivity.

The MTT assay was used to evaluate the vitality of the cells. Serial dilutions of the samples were applied to evaluate the viabilities of all BG specimens in accordance with the advised testing method ISO 10993-5. Prior to being diluted in one of five distinct extraction concentrations, 20%, 40%, 60%, 80%, or 100%, in minimum essential medium (MEM), the samples were first autoclave-sterilized. The seeded cells were grown in a 24-well plate with BG specimens at a density of 2104 cells/cm³ and the cells were then incubated for 24 hours at 37°C in a humidified environment of 95% air, as well as 5% CO₂. When the medium had been removed, 300 L of MTT reagent had been applied to each well. The plates then were positioned in a CO2 incubator and remained for 72 hours at 37°C. After aspirating the medium, 200 L dimethyl sulfoxide (DMSO) was added to each well. Then, the absorbance was assessed with microplate reader at a wavelength of 570 nm after the solution had been transferred to a 96-well plate (Multiskan Go, Thermo Scientific, USA). At last, the experimental method described by Kuo et al. was used to measure cell viability [23].

3. Results and Discussion

The TGA result of PEG, pure BG, and BG-derived PEG precursor was shown in Figure 1. As shown in Figure 1(a), at ∼400°C the sharp peak determines the PEG mass loss in the particles. For pure BG precursors, as shown in Figure 1(b) (inset 1) with the temperatures of ∼50 to ∼200°C and 550 up to 800°C can be assigned to removal of water, and calcium oxide formation, respectively. In addition, Figure 1(b) (inset 2) BG-derived PEG precursors demonstrated that even at 400°C, some PEG residues might still be present in particles. At 550°C, the next mass loss stage begins due to the decomposition of Ca(NO₃)₂ and at this temperature, no PEG is remaining in the particles.

(a)

(b)

PEG-derived BG powders have a specific surface area of 92.5 ± 0.3 and a pore volume of 0.27 ± 0.01 which are higher than those of pure BG (41.2 ± 0.1 for specific surface area and 0.22 ± 0.01 for pore volume) (Table 1). The data were expressed as mean standard deviation (SD) for n = 3. Both specimens showed a significant value at [31, 32]. The variation in the value indicates there is a substantial difference between the two BG samples.

Figure 2 depicts the surface morphologies of both BG powders by SEM images. Figure 2(a) illustrates that spherical and smooth surface morphology was obtained from solid BG powder. Similarly, the SEM images of the PEG-derived BG powder also exhibited spherical and smooth surface morphology, as seen in Figure 2(b).

EDS results in Figure 3 demonstrate the presence of silicon, calcium, and phosphorous peaks in both synthesized samples which were typical for any silicate bioactive glasses [31]. It also indicates absence of any residual PEG and other residual components which was successfully eliminated at the heating process.

(a)

(b)

The TEM images in Figure 4 show the inner structure for both BG particles. Figure 4(a), which depicts the pure BG powder, simply reveals the particles with continuous contrast, suggesting that there is not any thickness variance within the particles. As a result, it is able to be classified as a solid BG particle while Figure 4(b), shows hollow spheres that contains a single pore. In summary, when SEM and TEM pictures are combined, pure BG particles only have one solid sphere form, whereas PEG-derived BG particles have hollow particles.

Also, both BG powders were examined for in vitro bioactivity following a 12-hour soaking in SBF. Figure 5, shows the SEM images of both BG powders after immersing in SBF for 12 h. From the images, it is noticeable that each BGs powder’s surface had formed into the shape of a needle.

As Figure 5 illustrates, (inset) the Ca/P ratio was calculated from SEM-EDS spectra, and the higher Ca/P ratio was obtained for PEG derived-BG powders compared to pure BG powders which induce better in vitro bioactivity formation [5].

The solid and hollow BGs particle’s cell viability were evaluated by the MTT test [33, 34], and the results are seen in Figure 6. Cell viability was calculated as a percentage of cell viability at different extract concentrations. Figure 6 demonstrates that at extraction concentrations of 20%, 40%, 60%, 80%, and 100%, both BGs specimens (solid and hollow particles) passed the normal cell viability limit of 70%, demonstrating that all specimens were nontoxic. BG specimens with hollow particles were better in biocompatibility compared to solid particles in all extraction concentrations.

To express all data, the mean standard deviation (SD) for n = 3 was applied. As shown from Table 2, the p values for both solid and hollow particles at all extraction concentration were significant at .

It has been shown that both BG powders have spherical particle morphology depending on the SEM images presented in Figure 2. This is attributed to the “one particle per drop” or distinctive particle generation principle of the spray pyrolysis technique [27]. Moreover, it is clear from the TEM images shown in Figure 3 reveal that pure BG powders have solid structures, whereas PEG-derived BG powders exhibit hollow structures. Sequential PEG decomposition and BG particle precipitation are believed to be the mechanism of hollow particle generation. In addition, as seen in Figure 7, temperature rises may cause the PEG core to pyrolyze, leaving only the BGs shell.

4. Conclusions

In this work, solid and hollow spherical BG particle structures were successfully formed within spray pyrolyzed BGs. The EDS analysis revealed the formation of BGs with their respective elemental compositions. PEG-derived-BG powders have a larger specific surface area and performed better in bioactivity as compared to pure BG powders. Both the prepared powders were passing the minimum standard values of cell viability. From this study, the morphology directly influenced the bioactivity and biocompatibility of BG powders. Thus, it can be concluded that BGs with hollow spherical particles are a promising material for future tissue engineering development.

Data Availability

The data used to support the findings of this study are included in the article.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Authors’ Contributions

Fetene Fufa Bakare collected the data. Fetene Fufa Bakare, Tsion Chuni, Kena Dachasa, Fekadu Gochole, and Tadele Hunde performed data analysis and interpretation. Tsion Chuni wrote the original draft of the manuscript. Fetene Fufa Bakare and Tadele Hunde wrote, reviewed, and edited the manuscript. All authors read and approved the final manuscript.

Acknowledgments

The authors would like to acknowledge Adama Science and Technology University for funding. The authors also acknowledge the National Taiwan University of Science and Technology for materials support and characterization of the samples and cytotoxicity test.

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Copyright © 2023 Tsion Chuni et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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