The Effect of Different Substitutions (Cobalt, Copper, Strontium and Zinc) on the Properties of Akermanite Bioceramic: A Comparative Experimental Study

doi:10.21203/rs.3.rs-3263841/v1

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The Effect of Different Substitutions (Cobalt, Copper, Strontium and Zinc) on the Properties of Akermanite Bioceramic: A Comparative Experimental Study

https://doi.org/10.21203/rs.3.rs-3263841/v1

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Bioactive ceramics paly vital role in tissue engineering. One of the most important silicate base bioceramics is akermanite. In this research, the akermanite powder, was synthetized using sol-gel method and the effect of different substituents of Cobalt, Copper, Strontium and Zinc on its properties investigated. Results of Field Emission Scanning Electron Microscope (FESEM) observation and X-ray diffraction analysis (XRD), revealed that the substituents had significant effect on the morphology of powder particles of akermanite, and also the phases of samples. The results of 3-point bending test on sintered samples in cubic form, revealed that substituents affect the bending strength of akermanite, and highest strength were 97 MPa related to the Co- substituted akermanite. After soaking akermanite samples including different substituents in Simulated Body Fluid (SBF) for apatite forming ability measurement, the results of SEM observation, Energy dispersive spectroscopy (EDS) and XRD analysis revealed that all samples had appropriate apatite forming ability and Zn-substituted and unsubstituted akermanite samples had the highest. Also, the result of cell viability measurement via MTT test indicated that the Zn-substituted akermanite had the highest cell viability among all. Noting all results, the Zn-substituted akermanite had the optimum properties for bone tissue engineering.

Bioceramic

Silica-based

Bioactivity

Akermanite

Ion substitution

Commercialized bioactive ceramics (β-TCP and hydroxyapatite) have good biocompatibility and osteoconductivity and have been widely used for orthopedic and dental applications [1]. But low compressive strength and fracture toughness of β-TCP and its high degradation rate [2] and also low fracture toughness of hydroxyapatite [1], have led researchers to develop new bioceramics. Akermanite (Ca₂MgSi₂O₇) as a Mg-, Ca-, Si-based bioceramic is more bioactive and have faster new bone formation ability in vivo, and degradation rate than that of β-TCP [3]. Mg, Ca, Si-based bioceramics can be used as bone substitute [4], coating for metallic implants [5, 6, 7], reinforcement of polymeric biomaterials [8, 9], drug delivery [10, 11] and porous scaffolds [12, 13].

In all applications of bioceramics, it is expected to have appropriate mechanical properties, degradation rate, no toxicity or allergic effects, biocompatibility, bone-like apatite formation and good interactions with surrounding cells and tissues [14].

Silicate bioceramics are a new category of bioceramics which can release Si, Mg or Ca ions and improve the mineralization of extracellular matrices or cell response [12]. Akermanite is a Mg-, Ca-, Si- based bioceramic [15, 16] which include better degradation behavior than that of Mg, Si-based bioceramics [17]. Akermanite (Ca₂MgSi₂O₇) has appropriate in vitro apatite forming ability [18], and this ability is influenced by the surface roughness [19]. Akermanite is a biocompatible and biodegradable [20], and osteoinductive ceramic [21] which induce angiogenesis during bone regeneration [22]. Liu et al. reported that after 9 weeks of in vivo implantation, new bone formation of akermanite is 94% higher than that of β-TCP [17]. The degradation rate, ion release and pH change around the implant, affect the bone formation around it [17]. While the incorporation of Mg/Zn into silicate based bioceramics, can reduce the degradation rate [23]. Different researchers have tried to incorporate different substitutions in to the bioceramics to improve their properties.

Zhang et al. added different substituents to porous CaSiO₃ scaffold and stated that Mg containing substituents (MgSiO₃ and MgCl₂) increase the mechanical properties and decrease its degradation rate, while Ca containing dopant (CaSO₄) has reverse effect [24].

Mohammadi et al. incorporated strontium to the akermanite, and reported that strontium increased the mechanical properties of akermanite, while did not affect its bioactivity significantly [25]. Zirak et al. used different Mg, Ca and Si- based bioceramics of bredigite, akermanite, and diopside as drug carrier and reported their degradation rate as: bredigite > akermanite > diopside [10].

Akermanite can be fabricated using mechanical activation [15], sol-gel [18, 19], using food waste materials [27], but the sol-gel is a facile and exact method to incorporate different substitutions in to the bioceramics. So, in this research, using sol-gel method, different substitutions of cobalt, copper, and strontium are incorporated to the akermanite to develop a multi-functional bioceramic and the properties are studied comparatively.

2.1. Sample preparation

2.1.1. Synthesis of the akermanite powders including different substitutions

2.1.1. Synthesis of metal-akermanite (Ca2MSi2O7) bioceramics (Mg:Cu, Sr, Zn and Co)

The sol-gel method was used for synthesizing substituted akermanite bioceramics by using tetraethyl orthosilicate ((C₂H₅O)₄Si, TEOS), Magnesium nitrate hexahydrate (Mg(NO₃)₂. 6H₂O), Copper(II) nitrate trihydrate Cu(NO₃)₂. 3(H₂O), Zinc nitrate hexahydrate Zn(NO₃)₂. 6H₂O, Strontium nitrate (Sr(NO₃)₂) and Calcium nitrate tetrahydrate (Ca(NO₃)₂.4H₂O) as raw materials. The substituted akermanite bioceramics were prepared by first mixing 5.54 ml of the TEOS with deionized water (3.6 ml) and 0.1M HNO₃ (1.6 ml). Then the mixture was hydrolyzed for 30 min under stirring at room temperature. Thereafter, 25 mmol of Ca(NO₃)2.4H₂O and 12.5 mmol of M(NO₃).XH₂O (M: Mg, Co, Zn, Cu, Sr) were added to the mixture, and reactants were stirred for 5 h at room temperature. After the reaction, the solution was maintained at 60 ^oC for 1 day and dried at 120 ^oC for 2 days to obtain a dry gel. Afterward, the formed gels were calcined at 1200 ^oC for 3 h.

2.1.2. Fabrication of the akermanite bulks

The conventional powder metallurgy rout was used for bulk fabrication. Appropriate amount of each bioceramic powder was cold pressed in a cylindrical steel die (D = 8 mm, H = 8 mm) at a pressure of 400 MPa. Then the compacted pellets were heated at appropriate sintering temperature for 2 h. The heating and cooling rate were set on 5 °C/min.

2.2. Evaluation of the samples

2.2.1. Microscopic evaluation

Field emission scanning electron microscopy (FESEM, TESCAN MIRA3, Netherland) using secondary electron mode and energy dispersive spectroscopy (EDS) was utilized to study the size, morphology and elemental analysis of the akermanite particles and apatite forming ability.

2.2.2. X-ray diffraction (XRD) analysis

The X-ray diffraction (XRD, Philips X'Pert-MPD) was performed to evaluate the possible phases available in the akermanite particles and also apatite forming ability. The diffraction pattern was obtained by a Cu-Kα radiation source at a 1.54 A wavelength in the range of 20–80° and a step-size of 0.05^°.

2.2.3. Measuring the mechanical properties

In order to investigate and compare the mechanical properties of the sintered samples, cubic samples (2×4×10 mm) were used for 3-point bending test in accordance with the ASTM 1161-18 standard, using the universal testing machine (walter + bai ag, Switzerland) at a crosshead speed of 0.5 mm/min. The bending strength of sintered rigid samples was calculated using Eq. 1. The test was repeated 3 times for each sample and the average values are reported.

Equation (1):\(\sigma =\frac{3fl}{2B{D}^{2}}\)

where, σ is bending strength, f final applied force, l the length of sample, B the width and D the thickness of sample.

2.2.4. In vitro apatite forming ability assessment

The in vitro apatite forming ability as an approved criterion for bioactivity and bone bond ability was studied by soaking the samples into the simulated body fluid (SBF) at temperature of 37°C for 7 days according to the Kokubo’s protocol [22]. Then, the samples were taken out, gently rinsed with distilled water gently and the deposited apatite on the surfaces were observed by FESEM.

2.2.5. In vitro cell viability and attachment assay

For cell viability assessment, the MG-63 cells were seeded on the sterilized samples at a density of 1×10⁶ cells/sample and incubated at 37°C for 1, 3 and 7 days (n = 3). In addition to the sintered samples, a control group (a well without sample) was also assessed for compassion. Finally, the mediums were discarded and replaced by 500 µl MTT solution [3-(4,5-dimethylthiazol)-2,5-diphenyltetrazoliumbromide] and incubated for 4 h at 37°C. Then the solution was discarded and replaced by 500 µl dimethyl sulfoxide (DMSO). The spectrophotometrical absorbance of the specimens was measured using Elisa reader (Bio Rad, Model 680 instruments) at 490 nm emission wavelength and the cell viabilities were calculated using the Eq. (2).

Equation (2): Relative cell viability (%) = (A_s-A_b)/(A_c-A_b )

where A_b means absorbance of solution, A_c means absorbance of control sample, A_s means absorbance of sintered sample.

3.1. Particle size and morphology of powders

The FESEM micrograph of samples are presented in Fig. 1. According to this figure, it is evident that the morphology of synthetized samples differs from each other and the substituents affect the microstructure of samples effectively. The Co-substituted sample include nano-features (with the size of about 40 nm) on the surface and a few pores in the range of 800 nm. The Cu-substituted sample include sharp edge and flat surfaces (like cleavage fracture), while unsubstituted akermanite sample include porosity and also some nano-features in its structure. The microstructure of Sr-substituted, unsubstituted akermanite and Zn-substituted sample was almost the same, these tree samples include more porosities in their matrices than that of Cu or Co- substituted samples. By comparing the Fig. 1(C, D, E) it is evident that the pore size of unsubstituted akermanite, Sr-substituted and Zn-substituted samples was almost 500, 380 and 90 nm, respectively.

3.2. Phases analysis

Figure 2 presents the phases analysis of synthetized samples. According to the Fig. 2, the peaks of XRD pattern of akermanite are match with the JCPDS no of 96-900-6117, including Tetragonal crystal structure (Space group: P-421m, calculated density (g/cm³): 2.98). Also, Zn- substituted sample, unsubstituted sample and somewhat Co-substituted sample are match to this pattern. The strongest peak of the XRD spectra of these samples is located at 2θ of 31.25° and is related to the \(\left(211\right)\) atomic plane.

While the XRD patterns of Cu-substituted and Sr-substituted samples are not match to the JCPDS no of 96-900-6117, characteristic peaks of Ca₂SiO₄ crystallites were observed in the XRD patterns of the Sr-substituted sample (JCPDS card No. 96-900-610). It is evident that the XRD pattern of the Sr-substituted sample does not include any sharp and height peaks, and their patterns include broad peaks, implying high residual stress of atomic lattice. Also, the peaks evident at 23.17, 25.27, 26.85,28.85, 30.00, 35.57, 36.42, and 38.62° in the XRD spectra of the Cu-substituted sample match well with wollastonite (JCPDS card no: 043-1460).

3.3. Mechanical properties

The bending strength of Co-substituted, Cu-substituted, unsubstituted akermanite, Sr-substituted and Zn-substituted akermanite samples was measured using 3-point bending test. The results show that different substituents affect the mechanical properties of akermanite significantly. The bending strength were 97 ± 5, 92 ± 4, 88 ± 3, 81 ± 6 and 72 ± 5 MPa for Co-substituted, unsubstituted akermanite, Zn-substituted, Cu-substituted and Sr-substituted akermanite samples, respectively. It is evident that the highest bending strength is related to the Co-substituted akermanite and the lowest bending strength is related to the Sr-substituted akermanite. The mechanical properties can be affected by the different chemical bonds of substituents and other elements and also the residual stress of substitution atoms of substituents in crystal structure of akermanite. It seems the atomic radius (Table 1) of strontium is so larger than the other and this results to huge residual stress in crystal structure of akermanite, and affect the mechanical properties of akermanite, reversely. This phenomenon is observable in XRD pattern of Sr-substituted akermanite in Fig. 2, the graph does not have sharp and height peaks (related to crystalline materials).

The radius of atoms of Ca, Co, Cu, Mg, Sr and Zn are presented in Table 1.

Table 1

The radius of atoms of Ca, Co, Cu, Mg, Sr and Zn.
atom	Calcium	Cobalt	Copper	Magnesium	Strontium	Zinc
Radius (pm)	194	152	145	145	219	142

3.4. Apatite forming ability

After sample immersion in SBF for 7 days, the surface of samples was characterized using FESEM, EDS and XRD analysis. According to the Fig. 3, the surface of all samples was covered by particles after immersion in SBF. While, the morphology of depositions on the samples of Co-substituted, unsubstituted akermanite and Zn-substituted akermanite samples had cauliflower-like morphology, all depositions composed of Ca and P ions, indicating calcium phosphate deposition on all samples after immersion in SBF. Also, according to the results of EDS analysis, the intensity of Ca and P in unsubstituted akermanite and Zn-substituted samples was higher than the others. It seems, unsubstituted akermanite and Zn-substituted samples had higher apatite forming ability than the Co-substituted, Cu-substituted and Sr-substituted samples.

Figure 4 shows the phases analysis of samples after immersion in SBF. According to the Fig. 4, Zn-substituted akermanite have highest peaks related to hydroxyapatite (JCPS no.: 96-230-0274), which is in good agreement with results of SEM and EDS analysis.

3.5. In vitro cell behavior

3.5.1. Cell viability

The cytotoxicity of samples was evaluated by MTT assay on days 1 and 5 of L-929 cell culture. According to Fig. 5, cell viability for Zn-substituted, unsubstituted akermanite and Co-substituted samples increased over time, and cell viability for Sr-substituted and Cu-substituted samples decreased over time. Zn-substituted, unsubstituted akermanite, Sr-substituted and Co-substituted samples showed significantly higher cell viability than Cu-substituted sample (p < 0.001).

Among all samples, the Zn-substituted sample showed best cell viability than the others. Also, the rising manner of the cell viability of Zn-substituted sample by the time, is noticeable.

K. Bavya Devi et al. reported that Zn substituted forsterite (Mg₂SiO₄) have more degradation rate than that of pure forsterite (forsterite without any dopant), while both of them have almost same cell proliferation [27].

Salahinejad et al. stated that the sintering ability and apatite forming ability of diopside (CaMgSi₂O₆) improves by 1% mol F doping [28].

V. Giannoulatou et al. fabricated Mg-, Ca-, Si bioactive glass substituted with Cu to improve its properties [29].

It has been reported that Mg play an important role in human bone growth and repair by stimulating osteoblast proliferation [30]. Of course, Cu, Sr, Zn, Co, Si and B, have been used as potential therapeutic agents due to their ability to enhance bone formation due to their stimulating effects on both osteogenesis and angiogenesis [31–33], while Cu can be dopped successfully in akermanite, and considered as an angiogenesis element [34, 35].

While the bioactive ceramics are used in different forms of coating, filler of composites, porous scaffolds and bulk in tissue engineering, so modulating their properties is important. In this research for the first time, the effect of different substituents of Cobalt, Copper, Strontium and Zinc on the properties of akermanite investigated. Although all samples of Cobalt, Copper, Strontium and Zinc substituted akermanite had appropriate properties, but the Zinc substituted akermanite (Zn-substituted sample) was the optimum, and can be considered as a promising candidate for bone tissue engineering (of course after more in vitro cell studies and in vivo experiments).

Acknowledgment

This study was approved by Ethics Committee of Isfahan University of Medical Sciences (IR.MUI.RESEARCH.REC.1399.018) and fully supported by the Research Deputy of Isfahan University of Medical Sciences (Grant # 240065).

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No competing interests reported.

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The Effect of Different Substitutions (Cobalt, Copper, Strontium and Zinc) on the Properties of Akermanite Bioceramic: A Comparative Experimental Study

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Abstract

Figures

1. Introduction

2. Materials and methods

2.1. Sample preparation

2.1.1. Synthesis of the akermanite powders including different substitutions

2.1.1. Synthesis of metal-akermanite (Ca2MSi2O7) bioceramics (Mg:Cu, Sr, Zn and Co)

2.1.2. Fabrication of the akermanite bulks

2.2. Evaluation of the samples

2.2.1. Microscopic evaluation

2.2.2. X-ray diffraction (XRD) analysis

2.2.3. Measuring the mechanical properties

2.2.4. In vitro apatite forming ability assessment

2.2.5. In vitro cell viability and attachment assay

3. Results and discussion

3.1. Particle size and morphology of powders

3.2. Phases analysis

3.3. Mechanical properties

3.4. Apatite forming ability

3.5. In vitro cell behavior

3.5.1. Cell viability

4. Conclusion

Declarations

Acknowledgment

References

Additional Declarations

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