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Characterization, biocompatibility and in vivo of nominal MnO2-containing wollastonite glass-ceramic

  • Samah S. Eldera , Nourah Alsenany , Sarah Aldawsari , Gehan T. El-Bassyouni and Esmat M. A. Hamzawy EMAIL logo
Published/Copyright: September 13, 2022
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Nanotechnology Reviews
From the journal Nanotechnology Reviews Volume 11 Issue 1

Abstract

The present work pointed out the effect of adding different concentrations of MnO2 (0.25, 0.50, 1.00 and 2.00 wt%) on the structure and crystallization performance of wollastonite glass. Nominal MnO2-containing wollastonite glass was prepared with the addition of 10% Na2O to decrease the melting temperature through melt quenching technique. The thermal history of glasses indicated that the crystallization temperature was between 864 and 895°C. The heat treating of glasses at ∼900 and 1,100°C gave combeite (Na4Ca4Si6O18), rankinite (Ca3Si2O7), pseudowollastonite (Ca3Si3O9), bustamite (CaMnSi2O6) and cristobalite. The later sample densities increased with the incorporation of MnO2 from 1.88 to 2.24 g/cm3 concomitant with decrease of porosities from 32.59 to 20.83%. The microstructure showed nano-size crystals in rounded, angular or irregular micro-size clusters, whereas after soaking in simulated body fluid for 1 month showed submicron crystals of carbonated calcium phosphate phase. Both fourier transform infrared spectroscopy and scanning electron microscopy/energy dispersive X-ray delineated the samples’ biocompatibility. Also, the negative zeta potential results enabled bone cell activity. Moreover, the bone healing with complete mineralization was remarked in case of the in vivo implantation of the G0.50 group. These results can be of a great significance in the application of MnO2-containing combeite, rankinite phases for bone treatment and biomedical applications.

Keywords: glass-ceramic; biocompatibility; in vitro ; in vivo

1 Introduction

Wollastonite (Ca–Si-based bioceramic, CaSiO3) is an attractive candidate for bioengineering owing to the release of the Si4+ and Ca2+ ions upon degradation, such ions play a significant role in osteogenesis and angiogenesis. Wollastonite doped with bioactive elements is believed to be a good candidate for bone tissue engineering due to their amendable biodegradation and bioinductivity [1,2]. Doping of wollastonite with manganese (Mn2+) can fortify the capacity of the calcium silicate [3,4]. CaSiO3 has been premeditated as a bioactive material due to its excellent bioactivity and degradability [5]. Silicon and calcium act as a potential network modifier for the improvement of the bone substitutions by therapeutic inorganic ions during the early stages of bone development, mineralization and growth [6]. Their good biological properties are accredited to their capacity for alkalinizing activity and the release of calcium which is ideal for the calcium phosphate (Ca-P) nucleation [7]. Calcium silicate is an osteoinductive non-cytotoxic material [8,9].

Manganese dioxide (MnO2), is a non-stoichiometric inorganic material which added an important consideration in the material science field due to its distinctive physicochemical properties [10]. Among metal oxides, MnO2 has received a considerable attention because of its cost-effective, great activity, high stability, low toxicity, large specific surface area, flexible structure and strong oxidizing properties [11]. The dimensions, crystallographic phases, morphology and particle size are the unique physicochemical properties of the MnO2. Manganese can improve several functional materials as it fulfils the strict biomedical necessities [12]. Researchers, revealed that doping of MnO2 can improve the dielectric properties of ceramics [13,14]. The influence of MnO2 mostly impacts the microstructure and the energy storage properties of the calcium silicate. In 2017, Xiu et al. concluded that the addition of a small amount of MnO2 can improve the homogenization and densification of the ceramic material and subsequently improve its microstructure [15]. In 2016, Danewalia and Singh indicated that the existence of MnO2 increases the leakage of the Na+ ions from the glasses and likewise attracts the Ca2+ cations from the simulated body fluid (SBF) [16]. They similarly mentioned that the incidence of MnO2 may improve the glass surface activity to form an apatite layer. In 2015, Kolmas et al. noted that Mn-doping could increase the compressive strength and density of the scaffolds [17].

In the current research, nominal wollastonite glass-ceramic with various concentrations of MnO2 was prepared through the melt quench method. The produced manganese/wollastonite glasses were characterized in terms of morphology and composition via in vitro and in vivo bioactivity. Characterization of the glasses was obtained using differential thermal analysis (DTA), X-ray diffraction (XRD) and scanning electron microscope (SEM) coupled with energy dispersive X-ray microanalysis (EDX). For in vitro biocompatibility, glass powder was pressed into discs before immersion in SBF for 1 month. For the in vivo investigation, the base nominal wollastonite glass (G0), and those combined with 0.25 M and 0.50 M of MnO2 samples were implanted in the femur bone defects of hamster rats for 45–90 days to identify the new bone formation.

2 Experimentation

Wollastonite (CaSiO3) was prepared through the melt quench route. The influence of MnO2 (BDH) on the characterization and biocompatibility of the glass was investigated. The content of MnO2 in glass samples was 0.0, 0.25, 0.50. 1.00 and 2.00 wt%. To reduce the melting temperatures of the glass batches, 10% Na2O was added over the 100% glass oxide composition (Table 1). The glass batch constituents were pure limestone (LS contains CaO: 55.7, Al2O3: 0.22, Fe2O3: 0.02, MgO: 0.1, Na2O: 0.1, K2O: 0.16 and TiO2: 0.02 wt%) as the source of CaO; whereas, silica sand was used as the source of SiO2. Over 100% glass batch oxides were MnO2 (Sigma Aldrich, USA) and sodium carbonate (Na2CO3, BDH) as the source of Na2O. The melting temperature of the batches was between 1,350 and 1,400°C for 2 h in a platinum crucible. After adequate homogeneity, glass melt was poured into distilled water (at room temperature) before dryness and pulverization (<0.083 mm). The pulverized glass powder was shaped into discs of diameter 1.00 cm, using 7% poly vinyl alcohol as a binder, via Paul Weber Maschinen- und Apparatebau, Remshalden, Germany at 20 kN for 20 s.

Table 1

Chemical composition of the glass batches

Sample code Batch in oxides weight% Batch in gram
CaO SiO2 Over 100% addition Starting material
Na2O MnO2 LS Silica sand Na2CO3 MnO2
G0 48.28 51.72 10.00 00 86.68 51.72 17.00 0.00
G0.25M 48.28 51.72 10.00 0.25 86.68 51.72 17.00 0.25
G0.50M 48.28 51.72 10.00 0.50 86.68 51.72 17.00 0.50
G1.00M 48.28 51.72 10.00 1.00 86.68 51.72 17.00 1.00
G2.00M 48.28 51.72 10.00 2.00 86.68 51.72 17.00 2.00

DTA (Perkin Elmer DTA-7, USA) was used to trace the thermal behavior of the glasses, under argon gas condition and a heating rate of 10°C/min up to 1,000°C. Identification of the crystalline phases of glasses at 900 and 1,100°C was performed using XRD analysis (BRUKER, D8 ADVANCED CuO target, Germany) with CuKα radiations (λ = 1.54 Å). XRD patterns were recorded in the range of 2θ = 5–60°. The morphology and microcrystalline structure of samples were verified by SEM equipped with EDX (SEM/EDX, model FEJ Quanta 250 Fei, Holland) at operating voltage of 15 kV. Prior to the SEM measurements, fresh fractured samples were etched with the solution of 1 wt% HNO3 + 1 wt% HF to clear the outlines of the developed crystalline particles.

Standard in vitro bioactivity tests using SBF at 37°C were carried out upon incubation for 1 month. SBF has ion concentrations, pH and temperature almost identical to that of the human blood plasma [18].

SBF was prepared following Kokubo’s protocol by dissolving appropriate amounts of reagent-grade chemicals NaCl, NaHCO3, KCl, Na2HPO4, MgCl2·6H2O, Na2SO4, (CH2OH)3CNH2 and CaCl2·2H2O in deionized water [19,20]. To mimic the concentration of human blood plasma, 1 M of HCl and tris-hydroxymethyl amino methane [(CH2OH)3CNH2] was used to maintain the pH of SBF solution at 7.4 [21]. Bioactivity test was performed for sintered glass discs sintered at 1,100°C/2 h. Discs were immersed in sealed sterilized polyethylene boxes enclosing SBF for 1 month, at a constant ratio of sample to SBF volume without refreshing the solution throughout the immersion. At the end of the immersion period, discs were removed from the solution, rinsed with distilled water to stop the reaction, and then dried at room temperature. Discs were successively characterized using SEM/EDX and fourier transform infrared spectroscopy (FT-IR) reflection (Jasco, FT/IR-4600, USA) to detect the possible formation of the Ca-P crystals and to assess the microanalysis and the Ca/P ratio on the sample. Also, the Zetasizer ([Malvern Instrument Ltd, UK] fortified with a 633 nm laser) was used to determine the electrical surface charges on the sample powder. A well-dispersed sample in deionized water at temperature 25°C was caught for the measurement of the zeta potential (each measurement being the average of 12 runs).

For in vivo tests, the G0, G0.25M and G0.50M sintered glass-ceramic were implanted in the femur bone defects of hamster rats, besides a positive control (empty bone gap). Normal healing of the soft tissues was identified. All rats were healthy and did not show any signs of edema in the tissues all through the post-operative period.

After 45 and 90 days’ post-surgery, the animals were lacerated with an overdose of anesthesia, and both femurs were extracted, cleaned of soft tissues and soaked in 10% phosphate-buffered formalin for 7 days. The rat bones were prepared for histological evaluation via normal light microscope (Leica, model: DM 2500).

3 Results and discussion

3.1 Characterization of samples

The thermal behavior of the glasses is elucidated by means of DTA in Figure 1. The glass transition temperature is near 675°C and softening temperature near 685°C. Such small heat absorption may designate the occurrence of molecular relocation earlier than the glass crystallization. Exothermic peaks demonstrating the crystallization reaction are also revealed [22]. The crystallization temperature is between 864 and 872°C. The onset and offset temperatures of all the glasses crystallization are between 830 and 900°C, respectively. It is manifested that the incorporation of MnO2 in the wollastonite glass does not show noticeable changes in the temperature of the endothermic and exothermic effect.

Figure 1 DTA thermograms of the glasses heated up to 1,000°C.
Figure 1

DTA thermograms of the glasses heated up to 1,000°C.

XRD analysis of the sintered glasses near the crystallization temperature (at 900°C/2 h) is presented in Figure 2. It exhibits main crystalline phases of complex silicates. The crystallization of combeite (Na4Ca4Si6O18) particularly in the G0 (base) [23]; whereas the incorporation of MnO2 enhances the crystallization of both pseudowollastonite (CaSiO3) [24] and rankinite (Ca3Si2O7) [25]. At higher concentration of MnO2 content (i.e., in G2.00M), bustamite (Mn,Ca)3Si3O9 phase is indexed along with the later phases [26]. At higher temperature (1,100°C), the crystallization of rankinite and combeite is noticed as major phases with little cristobalite (SiO2) in all samples [27] (Figure 3). For the parent (G0) sample, the XRD pattern concurs with those reported in the previous work [28,29].

Figure 2 XRD of glasses heated at 900°C/2 h.
Figure 2

XRD of glasses heated at 900°C/2 h.

Figure 3 XRD of glasses heated at 1,100°C/2 h.
Figure 3

XRD of glasses heated at 1,100°C/2 h.

SEM of G0, G0.50M and G2.00M glasses sintered at 1,100°C/2 h are shown in Figure 4. G0 sample shows massive microstructure with some irregular clusters and very little pores. Subsequently at high magnification, connected rounded clusters appear in the range of the nano-size. Once a small amount of MnO2 is added, the microstructure of the sintered samples becomes more uniform and denser having a spheroidal morphology and disordered mesoporous structure [15]. The G0.50M and G2.00M samples present mesoporous glass together with a mix of irregular, angular and fine rod-like crystals with pores in between. At higher magnifications, the microstructure of the later crystals exposes nano-size crystals (30–100 nm) as shown in Figure 4. The EDX microanalysis of G0 indicates the integration of Na, Ca, Si and O. However, the EDX of the G0.50M and G2.00M glass samples confirms the incorporation of the manganese into the glassy matrix. Thus, it exhibits an indication of rankinite crystallization and due to the similarity of ionic radius of calcium and sodium, the possible replacement of Ca (116 pm) by Na (114 pm) may take place (Figure 5 and Table 2).

Figure 4 SEM micrographs of G0, G0.50M and G2.00M glasses sintered at 1,100°C/2 h.
Figure 4

SEM micrographs of G0, G0.50M and G2.00M glasses sintered at 1,100°C/2 h.

Figure 5 EDX microanalysis of G0, G0.50M and G2.00M glasses sintered at 1,100°C/2 h.
Figure 5

EDX microanalysis of G0, G0.50M and G2.00M glasses sintered at 1,100°C/2 h.

Table 2

EDX microanalysis of G0, G0.50M and G2.00M samples

Chemical constituents weight%
Na Ca Si Mn O
Nominal rankinite — 41.69 19.48 — 38.83
G0 2.66 57.68 15.73 — 23.93
G0.50M 2.52 42.5 17.65 1.71 35.62
G2.00M 4.19 30.73 19.2 0.83 45.04

3.2 Densities, porosities and zeta potential

The densities and porosities of the glass samples sintered at 1,100°C are demonstrated in Figure 6. Upon incorporation of MnO2, the densities of the samples relatively increase from 1.88 to 2.24 g/cm3 and the porosities relatively decrease from 32.59 to 20.83%. Although the pre-mentioned densities of rankinite (2.844 g/cm3), combeite (2.690 g/cm3) and cristobalite (2.33 g/cm3) are higher than the present results, it must be mentioned that the increase of the porosities initiate decrease in such values. It is notable that all samples create negative zeta potentials as presented in Table 3. Such negative zeta potentials may be mainly accredited to the negative charge of the samples. Zeta potential of the major combeite, rankinite, containing 0.00, 0.50 and 2.00% of MnO2 has a lower negative value compared to that of the pure parent material (G0). Negative zeta potential may possibly be a useful property for bone-derived appliance when fixed in bone containing viable cells and deliberated for in vivo test (Figure 7). Likewise, it is clear that the conductivity of the electrolyte increases with the increase in the MnO2 content. For that reason, it may possibly be concluded that the deposition of MnO2 leads to a reduction in the zeta potential [30]. The lower values of zeta potential of all investigated samples doped with MnO2 designate the incipient instability of the particles suspension. Scientists stated that the bioactivity of nanocomposite materials can be predicted by the zeta potential of nano-additives [31,32]. From the author’s point of view, the most motivating finding was a negative zeta potential to enable the bone cell activity.

Figure 6 Densities and porosities of the samples sintered at 1,100°C/2 h.
Figure 6

Densities and porosities of the samples sintered at 1,100°C/2 h.

Table 3

The zeta potential measurements

Sample/Notation Zeta potential (mV) Conductivity (mS/cm) Std. Dev.
G0 −40.3 0.0402 4.64
G0.50M −25.1 0.0574 4.61
G2.00M −27.0 0.0888 3.78
Figure 7 Zeta potential of G0, G0.50M and G2.00M glass samples sintered at 1,100°C/2 h.
Figure 7

Zeta potential of G0, G0.50M and G2.00M glass samples sintered at 1,100°C/2 h.

3.3 Biocompatibility

3.3.1 In vitro results

To check the biocompatibility of the glasses, in vitro tests by means of the SBF are carried out. SEM micrographs of G0, G0.50M and G2.00M discs sintered at 1,100°C/2 h are soaked in SBF for 4 weeks as shown in Figure 8. G0 sample displays a mix of irregular angular, rod-like crystals with pores in between; whereas, at high magnification rounded, sub-rounded and rod clusters in the nano-size range are scattered all over the sample. On the other hand, G0.50M and G2.00M samples expose fine plate-like crystals mounting on the surface of the immersed samples. As shown in Figure 8, the later plate-like crystals are associated with tiny crystals with little pores in between and at high magnification the later crystals display nano-size crystals between 100 and 200 nm. On high magnification, the microstructure of the G2.00M sample is modified by means of interlocked ribbon containing nano-tiny crystals on its edges. Furthermore, the development of agglomerates is as a consequence of the van der Waals interaction forces between the particles [33]. EDX microanalysis demonstrates a growth in the intensity of the P and Ca peaks together with carbon and decline in the intensity of the Si peaks of all samples, which reflect the deposition of carbonated calcium phosphates (c-CaPs) (Figure 9). Also, the Ca/P ratios were 2.17, 2.30 and 2.97 for G0, G0.50M and G2.00M, respectively. Coating of the material surfaces by Ca-P can be used to increase the biological responses and decrease the toxicity [34]. Ca-P may happen in crystalline and amorphous phases with variable stoichiometry [35]. The in vitro results improve the osteoblast adhesion on the Ca-Ps with elevation in Ca/P ratio (up to 2.9) [36]. In classical condition, as the pH value of SBF was kept constant at 7.40 (i.e., over the isoelectric point of the particles), the surface charge of the particles is of negative charge when immersed in SBF, which managed to adsorb the Ca2+ ions from the SBF solution and ultimately form a crystalline layer of calcium-enriched apatite. In Figure 8, the EDX microanalysis of G2.00M sample shows a minute release of Mn ions, which recommends using such sample as a vehicle for providing therapeutic manganese ions [37].

Figure 8 SEM micrographs of the G0, G0.50M and G2.00M glasses sintered at 1,100°C/2 h and soaked in SBF for a month.
Figure 8

SEM micrographs of the G0, G0.50M and G2.00M glasses sintered at 1,100°C/2 h and soaked in SBF for a month.

Figure 9 EDX microanalysis of G0, G0.50M and G2.00M glasses sintered at 1,100°C/2 h and soaked in SBF for a month.
Figure 9

EDX microanalysis of G0, G0.50M and G2.00M glasses sintered at 1,100°C/2 h and soaked in SBF for a month.

Danewalia and Singh [16] mentioned that the incidence of MnO2 proliferates the disordering, thus improving the glass surface activity to form an apatite layer. Such findings approve their fittingness for being applicable in bone tissue engineering. However, in the present work, the increase of the c-CaP ratio monitors the successive incorporation of the MnO2 into the glass network [16].

The in vitro bioactivity studies in SBF designate that samples could prompt the Ca-P layer and propose the opportunity of relating the Mn-modified sample for bone regeneration as comprehended in Figure 9. Earlier, it was informed that the induction of Ca-P layer on surfaces of the bioactive materials was extremely important for the incorporation of materials with normal bone tissue [38]. The steps of the Ca-P layer formation stages on samples surface in SBF may possibly be summarized in the next six steps [36]:

  1. Exchange of Ca2+ from the material surface with H+ or H3O+ in the SBF.

  2. Release of soluble silica in the form of silicic acid [Si(OH)4] into the SBF and the formation of several silanol (Si–OH) groups onto the immersed surface.

  3. Development of hydrated silica rich layer on account of re-polymerization and condensation of the Si–OH groups.

  4. Precipitation of the Ca2+ ions and the PO 4 3 − groups aboard of the silica rich layer; consequently, an amorphous layer of Ca-P was established on the surface.

  5. Evolution of the amorphous Ca-P (ACP) rich layer by enhancing more Ca2+ and PO 4 3 − groups from the SBF.

  6. The crystallization of ACP rich layer by insertion of OH− and CO 3 2 − anions from SBF and finally the yield of the hydroxyl carbonate Ca-P layer [39].

3.3.2 FT-IR reflection

FT-IR spectra in Figure 10 elucidate the characteristic vibrational bands of the hydroxyapatite (HA) in the G0 and G2.00M glass discs sintered at 1,100°C/2 h and soaked in SBF for a month. Bands at 941 and 561 cm−1 are related to the P–O bending mode of vibration of the HA. At higher Mn content, the 561 band is shifted to 546 cm−1 [40]. Other bands at 1,597 and 845 cm−1 match the carbonate groups of the HA [41]. Likewise, a hump present at the 681 cm−1 is related to the hydroxyl group of the HA. The band at 501 cm−1 is credited to the Si–O–Si symmetric bending mode in the silicate network [42]. The band at 845 cm−1 corresponds to the C–O stretching mode of vibration.

Figure 10 FTIR reflection spectra of G0 and G2.00M glass discs sintered 1,100°C/2 h and soaked in SBF for a month.
Figure 10

FTIR reflection spectra of G0 and G2.00M glass discs sintered 1,100°C/2 h and soaked in SBF for a month.

Thus it can be concluded that the characteristics of FT-IR reflection spectra in Figure 10 correspond to the development of the carbonated hydroxyapatite (c-HA) layer on the sintered glass-ceramic discs. Consequently, the major combeite, rankinite/MnO2 lead to the development of c-CaP on their surface after immersion in SBF, which is similarly confirmed by the SEM/EDX. Miola et al. concluded that the Mn-leaching test in SBF delineated inconsistent trends probably due to a re-precipitation of the manganese compounds during the process of bioactivity [37]. The study of the in vitro bioactivity designates that all samples are capable to form Ca-P layer above their surfaces as specified by the FT-IR reflection and the SEM/EDX analysis.

3.3.3 In vivo tests

The in vivo results are verified on G0, G0.25M and G0.50M sintered at 1,100°C/2 h, and the positive group (empty bone gap) is the reference for the pre-mentioned sintered samples. Samples are implanted in the femur bone defects of hamster rats, and the results are examined after 45 and 90 days.

Light microscopic examination after 45 days of bone tissues for the control group (Figure 11) reveals normal histology of compact and trabecular bone without any detectible alterations and the positive control group shows an area of bone necrosis with the existence of some newly formed bone tissue that showed an irregular calcification pattern. On the other hand, the bone defect in the (G0) group displays delayed healing with the existence of necrotic tissue filling the bone gap. However, the edges of the defect demonstrate proliferating osteoblasts (PO). The area of bone defect in both G0.25M and G0.50M groups is filled by necrosed tissue debris along with the applied formula as shown in Figure 11.

Figure 11 Microscopic examination of (a) normal bone, (b) positive control and sample containing sintered (c) G0, (d) G0.25M and (e) G0.50M samples. Both G0.25M and G0.50M samples show nearly normal bone after 45 days of implantation. NFB: new formed bone, NT: necrosed tissue and PO: proliferating osteoblasts.
Figure 11

Microscopic examination of (a) normal bone, (b) positive control and sample containing sintered (c) G0, (d) G0.25M and (e) G0.50M samples. Both G0.25M and G0.50M samples show nearly normal bone after 45 days of implantation. NFB: new formed bone, NT: necrosed tissue and PO: proliferating osteoblasts.

After 90 days of implantation, both the control and positive groups illustrate PO filling the defect area (Figure 12). In the same period, the G0 indicates new formed osteoid tissue filling the defect area with defective mineralization. Moreover, as shown in Figure 12, the G0.25M group elucidates an apparently normal bone tissue at the defect area and perfect bone healing with complete mineralization is noticed in the G0.50 group.

Figure 12 Light microscopic examination of (a) G0, (b) G0.25M and (c) G0.50M demonstrates nearly normal bone after 90 days of implantation. NFO: new formed osteoid.
Figure 12

Light microscopic examination of (a) G0, (b) G0.25M and (c) G0.50M demonstrates nearly normal bone after 90 days of implantation. NFO: new formed osteoid.

In general, no inflammation or endothelial swelling or granulation tissue or fibrotic tissue or any rejection in both tested samples is detected. The results show that although the treatment and formation of new bone tissues are slow in the G0 sample, it is fast in case of incorporation of the MnO2 in G0.25M and G0.50M sintered samples. The presence of the major combeite (Na4Ca4Si6O18) and rankinite (Ca3Si2O7) with/without MnO2, as the major phases, not only stimulates the bioactivity but also triggers the activation of the osteoblast cell.

4 Conclusion

Nominal wollastonite with the successive four additions of MnO2 (0.25, 0.50, 1,00 and 2.00  mol%) contents are synthesized through melt quenching route. The incorporation of MnO2 does not show much changes in the temperature of endothermic and exothermic effect. XRD analysis of the sintered glasses near the crystallization temperature (at 900°C/2 h) showed the crystallization of combeite, pseudowollastonite, rankinite, bustamite and cristobalite. At higher temperature (1,100°C) the crystallization of the major rankinite and combeite was noticed as major phases with little cristobalite. In the later samples, with incorporation of MnO2, the densities were increased from 1.88 to 2.24 g/cm3 and the porosities decreased from 32.59 to 20.83%. The negative zeta potential of the present samples could be a useful property enhancing attachment and proliferation of bone cells when fixed in bone containing viable cells. The SEM of samples shows a mix of irregular angular and rod-like crystals with very fine pores in between. At higher magnifications, the microstructure of the later crystals shows nano-size crystals (between 30 and 100 nm). Post-immersion in SBF for 1 month the surface of the samples was studied via SEM/EDX and FT-IR reflection. However, the EDX microanalysis reflected the possible formation of c-HA on the surfaces upon immersion. The in vivo results show that although the formation of new bone tissues was slow in the case of the G0 sample, it was fast in case of G0.25M and G0.50M samples (i.e., the incorporation of MnO2 improved the new bone formation). Such outcomes are important in the application of MnO2-containing wollastonite glass for bone treatment and biomedical applications.

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Acknowledgments

The authors extend their appreciation to the Deputyship for Research & Innovation, Ministry of Education in Saudi Arabia for funding this research work through project number (IFPHI-054-247-2020)” and King Abdulaziz University, DSR, Jeddah, Saudi Arabia.

  1. Funding information: Deputyship for Research & Innovation, Ministry of Education in Saudi Arabia through project number (IFPHI-054-247-2020)” and King Abdulaziz University, DSR, Jeddah, Saudi Arabia.

  2. Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Ethical statement: The in vivo research protocol was reviewed and approved by the Animal Care Committee of the National Research Centre (NRC), Egypt, which follows the guidelines of the National Institutes of Health Guide for Care and Use of Laboratory Animals (approval registration No. 16-254).

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Received: 2022-01-24
Revised: 2022-03-26
Accepted: 2022-08-01
Published Online: 2022-09-13

© 2022 Samah S. Eldera et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/ntrev-2022-0477
Keywords for this article
glass-ceramic; biocompatibility; in vitro; in vivo
Creative Commons
BY 4.0

Articles in the same Issue

  1. Research Articles
  2. Theoretical and experimental investigation of MWCNT dispersion effect on the elastic modulus of flexible PDMS/MWCNT nanocomposites
  3. Mechanical, morphological, and fracture-deformation behavior of MWCNTs-reinforced (Al–Cu–Mg–T351) alloy cast nanocomposites fabricated by optimized mechanical milling and powder metallurgy techniques
  4. Flammability and physical stability of sugar palm crystalline nanocellulose reinforced thermoplastic sugar palm starch/poly(lactic acid) blend bionanocomposites
  5. Glutathione-loaded non-ionic surfactant niosomes: A new approach to improve oral bioavailability and hepatoprotective efficacy of glutathione
  6. Relationship between mechano-bactericidal activity and nanoblades density on chemically strengthened glass
  7. In situ regulation of microstructure and microwave-absorbing properties of FeSiAl through HNO3 oxidation
  8. Research on a mechanical model of magnetorheological fluid different diameter particles
  9. Nanomechanical and dynamic mechanical properties of rubber–wood–plastic composites
  10. Investigative properties of CeO2 doped with niobium: A combined characterization and DFT studies
  11. Miniaturized peptidomimetics and nano-vesiculation in endothelin types through probable nano-disk formation and structure property relationships of endothelins’ fragments
  12. N/S co-doped CoSe/C nanocubes as anode materials for Li-ion batteries
  13. Synergistic effects of halloysite nanotubes with metal and phosphorus additives on the optimal design of eco-friendly sandwich panels with maximum flame resistance and minimum weight
  14. Octreotide-conjugated silver nanoparticles for active targeting of somatostatin receptors and their application in a nebulized rat model
  15. Controllable morphology of Bi2S3 nanostructures formed via hydrothermal vulcanization of Bi2O3 thin-film layer and their photoelectrocatalytic performances
  16. Development of (−)-epigallocatechin-3-gallate-loaded folate receptor-targeted nanoparticles for prostate cancer treatment
  17. Enhancement of the mechanical properties of HDPE mineral nanocomposites by filler particles modulation of the matrix plastic/elastic behavior
  18. Effect of plasticizers on the properties of sugar palm nanocellulose/cinnamon essential oil reinforced starch bionanocomposite films
  19. Optimization of nano coating to reduce the thermal deformation of ball screws
  20. Preparation of efficient piezoelectric PVDF–HFP/Ni composite films by high electric field poling
  21. MHD dissipative Casson nanofluid liquid film flow due to an unsteady stretching sheet with radiation influence and slip velocity phenomenon
  22. Effects of nano-SiO2 modification on rubberised mortar and concrete with recycled coarse aggregates
  23. Mechanical and microscopic properties of fiber-reinforced coal gangue-based geopolymer concrete
  24. Effect of morphology and size on the thermodynamic stability of cerium oxide nanoparticles: Experiment and molecular dynamics calculation
  25. Mechanical performance of a CFRP composite reinforced via gelatin-CNTs: A study on fiber interfacial enhancement and matrix enhancement
  26. A practical review over surface modification, nanopatterns, emerging materials, drug delivery systems, and their biophysiochemical properties for dental implants: Recent progresses and advances
  27. HTR: An ultra-high speed algorithm for cage recognition of clathrate hydrates
  28. Effects of microalloying elements added by in situ synthesis on the microstructure of WCu composites
  29. A highly sensitive nanobiosensor based on aptamer-conjugated graphene-decorated rhodium nanoparticles for detection of HER2-positive circulating tumor cells
  30. Progressive collapse performance of shear strengthened RC frames by nano CFRP
  31. Core–shell heterostructured composites of carbon nanotubes and imine-linked hyperbranched polymers as metal-free Li-ion anodes
  32. A Galerkin strategy for tri-hybridized mixture in ethylene glycol comprising variable diffusion and thermal conductivity using non-Fourier’s theory
  33. Simple models for tensile modulus of shape memory polymer nanocomposites at ambient temperature
  34. Preparation and morphological studies of tin sulfide nanoparticles and use as efficient photocatalysts for the degradation of rhodamine B and phenol
  35. Polyethyleneimine-impregnated activated carbon nanofiber composited graphene-derived rice husk char for efficient post-combustion CO2 capture
  36. Electrospun nanofibers of Co3O4 nanocrystals encapsulated in cyclized-polyacrylonitrile for lithium storage
  37. Pitting corrosion induced on high-strength high carbon steel wire in high alkaline deaerated chloride electrolyte
  38. Formulation of polymeric nanoparticles loaded sorafenib; evaluation of cytotoxicity, molecular evaluation, and gene expression studies in lung and breast cancer cell lines
  39. Engineered nanocomposites in asphalt binders
  40. Influence of loading voltage, domain ratio, and additional load on the actuation of dielectric elastomer
  41. Thermally induced hex-graphene transitions in 2D carbon crystals
  42. The surface modification effect on the interfacial properties of glass fiber-reinforced epoxy: A molecular dynamics study
  43. Molecular dynamics study of deformation mechanism of interfacial microzone of Cu/Al2Cu/Al composites under tension
  44. Nanocolloid simulators of luminescent solar concentrator photovoltaic windows
  45. Compressive strength and anti-chloride ion penetration assessment of geopolymer mortar merging PVA fiber and nano-SiO2 using RBF–BP composite neural network
  46. Effect of 3-mercapto-1-propane sulfonate sulfonic acid and polyvinylpyrrolidone on the growth of cobalt pillar by electrodeposition
  47. Dynamics of convective slippery constraints on hybrid radiative Sutterby nanofluid flow by Galerkin finite element simulation
  48. Preparation of vanadium by the magnesiothermic self-propagating reduction and process control
  49. Microstructure-dependent photoelectrocatalytic activity of heterogeneous ZnO–ZnS nanosheets
  50. Cytotoxic and pro-inflammatory effects of molybdenum and tungsten disulphide on human bronchial cells
  51. Improving recycled aggregate concrete by compression casting and nano-silica
  52. Chemically reactive Maxwell nanoliquid flow by a stretching surface in the frames of Newtonian heating, nonlinear convection and radiative flux: Nanopolymer flow processing simulation
  53. Nonlinear dynamic and crack behaviors of carbon nanotubes-reinforced composites with various geometries
  54. Biosynthesis of copper oxide nanoparticles and its therapeutic efficacy against colon cancer
  55. Synthesis and characterization of smart stimuli-responsive herbal drug-encapsulated nanoniosome particles for efficient treatment of breast cancer
  56. Homotopic simulation for heat transport phenomenon of the Burgers nanofluids flow over a stretching cylinder with thermal convective and zero mass flux conditions
  57. Incorporation of copper and strontium ions in TiO2 nanotubes via dopamine to enhance hemocompatibility and cytocompatibility
  58. Mechanical, thermal, and barrier properties of starch films incorporated with chitosan nanoparticles
  59. Mechanical properties and microstructure of nano-strengthened recycled aggregate concrete
  60. Glucose-responsive nanogels efficiently maintain the stability and activity of therapeutic enzymes
  61. Tunning matrix rheology and mechanical performance of ultra-high performance concrete using cellulose nanofibers
  62. Flexible MXene/copper/cellulose nanofiber heat spreader films with enhanced thermal conductivity
  63. Promoted charge separation and specific surface area via interlacing of N-doped titanium dioxide nanotubes on carbon nitride nanosheets for photocatalytic degradation of Rhodamine B
  64. Elucidating the role of silicon dioxide and titanium dioxide nanoparticles in mitigating the disease of the eggplant caused by Phomopsis vexans, Ralstonia solanacearum, and root-knot nematode Meloidogyne incognita
  65. An implication of magnetic dipole in Carreau Yasuda liquid influenced by engine oil using ternary hybrid nanomaterial
  66. Robust synthesis of a composite phase of copper vanadium oxide with enhanced performance for durable aqueous Zn-ion batteries
  67. Tunning self-assembled phases of bovine serum albumin via hydrothermal process to synthesize novel functional hydrogel for skin protection against UVB
  68. A comparative experimental study on damping properties of epoxy nanocomposite beams reinforced with carbon nanotubes and graphene nanoplatelets
  69. Lightweight and hydrophobic Ni/GO/PVA composite aerogels for ultrahigh performance electromagnetic interference shielding
  70. Research on the auxetic behavior and mechanical properties of periodically rotating graphene nanostructures
  71. Repairing performances of novel cement mortar modified with graphene oxide and polyacrylate polymer
  72. Closed-loop recycling and fabrication of hydrophilic CNT films with high performance
  73. Design of thin-film configuration of SnO2–Ag2O composites for NO2 gas-sensing applications
  74. Study on stress distribution of SiC/Al composites based on microstructure models with microns and nanoparticles
  75. PVDF green nanofibers as potential carriers for improving self-healing and mechanical properties of carbon fiber/epoxy prepregs
  76. Osteogenesis capability of three-dimensionally printed poly(lactic acid)-halloysite nanotube scaffolds containing strontium ranelate
  77. Silver nanoparticles induce mitochondria-dependent apoptosis and late non-canonical autophagy in HT-29 colon cancer cells
  78. Preparation and bonding mechanisms of polymer/metal hybrid composite by nano molding technology
  79. Damage self-sensing and strain monitoring of glass-reinforced epoxy composite impregnated with graphene nanoplatelet and multiwalled carbon nanotubes
  80. Thermal analysis characterisation of solar-powered ship using Oldroyd hybrid nanofluids in parabolic trough solar collector: An optimal thermal application
  81. Pyrene-functionalized halloysite nanotubes for simultaneously detecting and separating Hg(ii) in aqueous media: A comprehensive comparison on interparticle and intraparticle excimers
  82. Fabrication of self-assembly CNT flexible film and its piezoresistive sensing behaviors
  83. Thermal valuation and entropy inspection of second-grade nanoscale fluid flow over a stretching surface by applying Koo–Kleinstreuer–Li relation
  84. Mechanical properties and microstructure of nano-SiO2 and basalt-fiber-reinforced recycled aggregate concrete
  85. Characterization and tribology performance of polyaniline-coated nanodiamond lubricant additives
  86. Combined impact of Marangoni convection and thermophoretic particle deposition on chemically reactive transport of nanofluid flow over a stretching surface
  87. Spark plasma extrusion of binder free hydroxyapatite powder
  88. An investigation on thermo-mechanical performance of graphene-oxide-reinforced shape memory polymer
  89. Effect of nanoadditives on the novel leather fiber/recycled poly(ethylene-vinyl-acetate) polymer composites for multifunctional applications: Fabrication, characterizations, and multiobjective optimization using central composite design
  90. Design selection for a hemispherical dimple core sandwich panel using hybrid multi-criteria decision-making methods
  91. Improving tensile strength and impact toughness of plasticized poly(lactic acid) biocomposites by incorporating nanofibrillated cellulose
  92. Green synthesis of spinel copper ferrite (CuFe2O4) nanoparticles and their toxicity
  93. The effect of TaC and NbC hybrid and mono-nanoparticles on AA2024 nanocomposites: Microstructure, strengthening, and artificial aging
  94. Excited-state geometry relaxation of pyrene-modified cellulose nanocrystals under UV-light excitation for detecting Fe3+
  95. Effect of CNTs and MEA on the creep of face-slab concrete at an early age
  96. Effect of deformation conditions on compression phase transformation of AZ31
  97. Application of MXene as a new generation of highly conductive coating materials for electromembrane-surrounded solid-phase microextraction
  98. A comparative study of the elasto-plastic properties for ceramic nanocomposites filled by graphene or graphene oxide nanoplates
  99. Encapsulation strategies for improving the biological behavior of CdS@ZIF-8 nanocomposites
  100. Biosynthesis of ZnO NPs from pumpkin seeds’ extract and elucidation of its anticancer potential against breast cancer
  101. Preliminary trials of the gold nanoparticles conjugated chrysin: An assessment of anti-oxidant, anti-microbial, and in vitro cytotoxic activities of a nanoformulated flavonoid
  102. Effect of micron-scale pores increased by nano-SiO2 sol modification on the strength of cement mortar
  103. Fractional simulations for thermal flow of hybrid nanofluid with aluminum oxide and titanium oxide nanoparticles with water and blood base fluids
  104. The effect of graphene nano-powder on the viscosity of water: An experimental study and artificial neural network modeling
  105. Development of a novel heat- and shear-resistant nano-silica gelling agent
  106. Characterization, biocompatibility and in vivo of nominal MnO2-containing wollastonite glass-ceramic
  107. Entropy production simulation of second-grade magnetic nanomaterials flowing across an expanding surface with viscidness dissipative flux
  108. Enhancement in structural, morphological, and optical properties of copper oxide for optoelectronic device applications
  109. Aptamer-functionalized chitosan-coated gold nanoparticle complex as a suitable targeted drug carrier for improved breast cancer treatment
  110. Performance and overall evaluation of nano-alumina-modified asphalt mixture
  111. Analysis of pure nanofluid (GO/engine oil) and hybrid nanofluid (GO–Fe3O4/engine oil): Novel thermal and magnetic features
  112. Synthesis of Ag@AgCl modified anatase/rutile/brookite mixed phase TiO2 and their photocatalytic property
  113. Mechanisms and influential variables on the abrasion resistance hydraulic concrete
  114. Synergistic reinforcement mechanism of basalt fiber/cellulose nanocrystals/polypropylene composites
  115. Achieving excellent oxidation resistance and mechanical properties of TiB2–B4C/carbon aerogel composites by quick-gelation and mechanical mixing
  116. Microwave-assisted sol–gel template-free synthesis and characterization of silica nanoparticles obtained from South African coal fly ash
  117. Pulsed laser-assisted synthesis of nano nickel(ii) oxide-anchored graphitic carbon nitride: Characterizations and their potential antibacterial/anti-biofilm applications
  118. Effects of nano-ZrSi2 on thermal stability of phenolic resin and thermal reusability of quartz–phenolic composites
  119. Benzaldehyde derivatives on tin electroplating as corrosion resistance for fabricating copper circuit
  120. Mechanical and heat transfer properties of 4D-printed shape memory graphene oxide/epoxy acrylate composites
  121. Coupling the vanadium-induced amorphous/crystalline NiFe2O4 with phosphide heterojunction toward active oxygen evolution reaction catalysts
  122. Graphene-oxide-reinforced cement composites mechanical and microstructural characteristics at elevated temperatures
  123. Gray correlation analysis of factors influencing compressive strength and durability of nano-SiO2 and PVA fiber reinforced geopolymer mortar
  124. Preparation of layered gradient Cu–Cr–Ti alloy with excellent mechanical properties, thermal stability, and electrical conductivity
  125. Recovery of Cr from chrome-containing leather wastes to develop aluminum-based composite material along with Al2O3 ceramic particles: An ingenious approach
  126. Mechanisms of the improved stiffness of flexible polymers under impact loading
  127. Anticancer potential of gold nanoparticles (AuNPs) using a battery of in vitro tests
  128. Review Articles
  129. Proposed approaches for coronaviruses elimination from wastewater: Membrane techniques and nanotechnology solutions
  130. Application of Pickering emulsion in oil drilling and production
  131. The contribution of microfluidics to the fight against tuberculosis
  132. Graphene-based biosensors for disease theranostics: Development, applications, and recent advancements
  133. Synthesis and encapsulation of iron oxide nanorods for application in magnetic hyperthermia and photothermal therapy
  134. Contemporary nano-architectured drugs and leads for ανβ3 integrin-based chemotherapy: Rationale and retrospect
  135. State-of-the-art review of fabrication, application, and mechanical properties of functionally graded porous nanocomposite materials
  136. Insights on magnetic spinel ferrites for targeted drug delivery and hyperthermia applications
  137. A review on heterogeneous oxidation of acetaminophen based on micro and nanoparticles catalyzed by different activators
  138. Early diagnosis of lung cancer using magnetic nanoparticles-integrated systems
  139. Advances in ZnO: Manipulation of defects for enhancing their technological potentials
  140. Efficacious nanomedicine track toward combating COVID-19
  141. A review of the design, processes, and properties of Mg-based composites
  142. Green synthesis of nanoparticles for varied applications: Green renewable resources and energy-efficient synthetic routes
  143. Two-dimensional nanomaterial-based polymer composites: Fundamentals and applications
  144. Recent progress and challenges in plasmonic nanomaterials
  145. Apoptotic cell-derived micro/nanosized extracellular vesicles in tissue regeneration
  146. Electronic noses based on metal oxide nanowires: A review
  147. Framework materials for supercapacitors
  148. An overview on the reproductive toxicity of graphene derivatives: Highlighting the importance
  149. Antibacterial nanomaterials: Upcoming hope to overcome antibiotic resistance crisis
  150. Research progress of carbon materials in the field of three-dimensional printing polymer nanocomposites
  151. A review of atomic layer deposition modelling and simulation methodologies: Density functional theory and molecular dynamics
  152. Recent advances in the preparation of PVDF-based piezoelectric materials
  153. Recent developments in tensile properties of friction welding of carbon fiber-reinforced composite: A review
  154. Comprehensive review of the properties of fly ash-based geopolymer with additive of nano-SiO2
  155. Perspectives in biopolymer/graphene-based composite application: Advances, challenges, and recommendations
  156. Graphene-based nanocomposite using new modeling molecular dynamic simulations for proposed neutralizing mechanism and real-time sensing of COVID-19
  157. Nanotechnology application on bamboo materials: A review
  158. Recent developments and future perspectives of biorenewable nanocomposites for advanced applications
  159. Nanostructured lipid carrier system: A compendium of their formulation development approaches, optimization strategies by quality by design, and recent applications in drug delivery
  160. 3D printing customized design of human bone tissue implant and its application
  161. Design, preparation, and functionalization of nanobiomaterials for enhanced efficacy in current and future biomedical applications
  162. A brief review of nanoparticles-doped PEDOT:PSS nanocomposite for OLED and OPV
  163. Nanotechnology interventions as a putative tool for the treatment of dental afflictions
  164. Recent advancements in metal–organic frameworks integrating quantum dots (QDs@MOF) and their potential applications
  165. A focused review of short electrospun nanofiber preparation techniques for composite reinforcement
  166. Microstructural characteristics and nano-modification of interfacial transition zone in concrete: A review
  167. Latest developments in the upconversion nanotechnology for the rapid detection of food safety: A review
  168. Strategic applications of nano-fertilizers for sustainable agriculture: Benefits and bottlenecks
  169. Molecular dynamics application of cocrystal energetic materials: A review
  170. Synthesis and application of nanometer hydroxyapatite in biomedicine
  171. Cutting-edge development in waste-recycled nanomaterials for energy storage and conversion applications
  172. Biological applications of ternary quantum dots: A review
  173. Nanotherapeutics for hydrogen sulfide-involved treatment: An emerging approach for cancer therapy
  174. Application of antibacterial nanoparticles in orthodontic materials
  175. Effect of natural-based biological hydrogels combined with growth factors on skin wound healing
  176. Nanozymes – A route to overcome microbial resistance: A viewpoint
  177. Recent developments and applications of smart nanoparticles in biomedicine
  178. Contemporary review on carbon nanotube (CNT) composites and their impact on multifarious applications
  179. Interfacial interactions and reinforcing mechanisms of cellulose and chitin nanomaterials and starch derivatives for cement and concrete strength and durability enhancement: A review
  180. Diamond-like carbon films for tribological modification of rubber
  181. Layered double hydroxides (LDHs) modified cement-based materials: A systematic review
  182. Recent research progress and advanced applications of silica/polymer nanocomposites
  183. Modeling of supramolecular biopolymers: Leading the in silico revolution of tissue engineering and nanomedicine
  184. Recent advances in perovskites-based optoelectronics
  185. Biogenic synthesis of palladium nanoparticles: New production methods and applications
  186. A comprehensive review of nanofluids with fractional derivatives: Modeling and application
  187. Electrospinning of marine polysaccharides: Processing and chemical aspects, challenges, and future prospects
  188. Electrohydrodynamic printing for demanding devices: A review of processing and applications
  189. Rapid Communications
  190. Structural material with designed thermal twist for a simple actuation
  191. Recent advances in photothermal materials for solar-driven crude oil adsorption
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