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Vol. 8. Issue 3.
Pages 2481-3388 (May - June 2019)
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Vol. 8. Issue 3.
Pages 2481-3388 (May - June 2019)
Original Article
DOI: 10.1016/j.jmrt.2019.04.001
Open Access
Mullite cytotoxicity and cell adhesion studies
Leandro Fernandesa, Renata Aquino de Carvalhob, Andre Capaldo Amaralb, Edison Pecoraroc, Rafael Salomãoa, Eliane Trovattib,
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Corresponding author.
a Materials Engineering Department – São Carlos School of Engineering, University of São Paulo, Avenida Trabalhador São-carlense 400, CEP: 13566-590, São Carlos, SP, Brazil
b University of Araraquara – UNIARA, Rua Carlos Gomes, 1217, CEP: 14801-340, Araraquara, SP, Brazil
c São Paulo State University (UNESP), Institute of Chemistry, CEP: 14800-060, Araraquara, SP, Brazil
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Figures (6)
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Tables (2)
Table 1. Characteristics of raw materials.
Table 2. Mechanical properties of mullite.
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Mullite is a low cost ceramic material based on aluminous silicate and synthesized via solid state reaction. Mullite displays potential properties for application in the biomedical field, specially its high mechanical strength, however it is poorly characterized with respect to its specific cytotoxicity and capability to allow the cell adhesion to its surface. Here, mullite was prepared by sintering the mixture of Al2O3 and SiO2 at 1500°C and characterized. Its elastic modulus was 135GPa and its flexural strength, 109MPa. The study of the viability of GM07492 human cells in presence of mullite revealed the proliferation and adhesion of the cells on its surface, which is an indication of biocompatibility. Its good mechanical properties and cytocompatibility suggested that mullite can be used as an alternative material for biomedical applications and dentistry.

Human cell
Cytotoxicity studies
Adhesion tests
Mechanical properties
Full Text

Ceramic materials have been extensively used in medicine due to their biocompatibility, high stiffness and compression strength ideal for use in orthopedic implants. Classical examples of ceramics used for bone replacement are alumina (Al2O3) [1,2] and zirconium dioxide (ZrO2) based biomaterials [3–6]. Al2O3 is an important commercially available biomaterial, however its low fracture toughness represents a great drawback. ZrO2 undergoes aging at body temperature in liquid medium, which limit its use in internal prostheses [7–9]. Although their association generate several devices for medical use (mainly for bone replacement), clinical data in orthopedics have demonstrated the need to develop new biomaterials with improved properties for good long-term performance [10–13].

Mullite (3Al2O3·2SiO2) is a low cost aluminous silicate with 71.8wt% Al2O3 and 28.2wt% SiO2[14], representing one of the main raw materials for the ceramic industry. Its application for development of new products for biomedical use is a strategy to decrease the costs, which also overcome the limitation [15]. Mullite is the result of the treatment of silica (SiO2) and alumina (Al2O3) [16] at temperatures above 1200°C forming its typical crystalline phase. Many sources of SiO2 can be used for mullite synthesis, including the SiO2 extracted from the silicon elemental purification process, a high available raw material, also known as microsilica. Usually mullite is found in applications that require high mechanical strength and high melting point, such as refractory materials [17,18], catalysts and filters in general [19,20]. Mullite avoids crack because it does not display phase transitions and volume expansion. This feature overcomes the drawbacks of conventional ceramics, which shows phase transition and can crack when expand [21].

Mullite derivatives have arisen for applications in medicine [22]. For instance, the apatite–mullite glass-ceramic [23] produced via selective laser sintering allowed bone growth into its porous structure after implanting in rabbit tibiae for four weeks [24]. The material did not show in vitro cytotoxic effect for the human dermal fibroblasts [25]. In another study, the biphasic composite based on mullite and calcium phosphate led to good cell viability, proliferation, and osteoblastic differentiation, which suggests it could be used for orthopedic applications [22]. Hydroxyapatite–mullite ceramic material, another mullite derivative induced cytotoxic and genotoxic activity against L929 mouse fibroblast cells. The authors attributed the negative effect to the particle size, concentration and composition of mullite [26]. All the mullite derivatives are glass ceramic based on calcium and/or phosphate salts found in the biological environment that perform biological holes, resulting in bioactive surface materials, which can improve their biological compatibility. However, their mechanical properties are decreased by these salts in their formulations. The compromise between mechanical properties and biocompatibility is crucial for materials designed for biomedical applications. Mullite shows good mechanical properties, avoids cracks and is expected to be inert. This is a good combination of properties for its use in the development of materials for biological purposes. Although, to the best of our knowledge, its biological properties, such as cytotoxicity and cell adhesion is not described in the literature, encouraging the development of this work.

In this study, mullite was synthetized from synthetic amorphous silica associated with calcined alumina and characterized for biomedical applications. The in vitro biocompatibility was accessed testing the viability of human cells in the presence of mullite by MTT cytotoxicity assay, and the adhesion of human cells on the surface of the material. The in vitro cytotoxicity assays were studied here as the first level of evidence tests for biomedical applications of mullite.

2Materials and methods2.1Materials

The materials used for the preparation of the mullite were (a) alumina (A1000SG, Almatis, Germany), (b) amorphous silica obtained by steam precipitation of elemental silicon (Microsilica 971, Elkem, Norway), organic binder (PVB; Polyvinyl butyral, Butivar® 98, Sigma-Aldrich, USA) and isopropyl alcohol (Synth; Brazil). The materials used for the biological tests were Dulbecco's modified eagle's medium (DMEM) and fetal bovine serum (Nutricell) purchased from (Gibco/Thermofisher), penicillin and streptomycin 10U/mL (Sigma Aldrich), 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium salt (MTT) from Merck, isopropyl alcohol, dimethyl sulfoxide, sodium hydroxide, sodium hypochlorite (NaClO) and phosphate buffer saline (PBS) purchased from Synth; trypsin from Gibco, 4,6-Diamidino-2-phenylindole (DAPI) and fluorescein isothiocyanate (FITC) from Sigma Aldrich. All solvents and reagents (analytical grade) were used as purchased. GM07492 cell line (human fibroblast primary cell line) was purchased from GM07492 Coriell Cell Repository (NIGMS Human Genetic Cell Repository), New Jersey, USA.

2.2Methods2.2.1Preparation and characterization of mullite

Dried silica and alumina were mixed in a stoichiometric proportion and dispersed in 2wt% PVB solution in isopropyl alcohol to form a suspension containing 33wt% of solids for the mullite formulation (3Al2O3·2SiO2). The suspension was poured into a high density polyethylene flask (2L) for grinding with zirconia spheres (5mm diameter, mass ratio of sphere: powder 10:1) at 90rpm for 2h. Isopropyl alcohol evaporated and the powder with PVB binder was de-agglomerated (Dpart<100μm) and pressed under uniaxial compression at 40MPa for generating bars (6×20×70mm) and cylinders (13mm diameter×3mm width). A heating treatment was applied at 5°Cmin−1 heating rate, hold at 1500°C for 3h; cooling rate of 10°Cmin−1. The scheme of the mullite preparation is shown in Fig. 1.

Fig. 1.

Scheme of the experimental procedure of mullite preparation and characterization.


The flexural elastic modulus of the mullite samples was determined by the impulse excitation technique (Sonelastic equipment, PTCA, Brazil) according to ASTM C 1198-91. The flexural modulus of rupture at three points was carried out in a universal testing machine (Model WDW-30E, China) equipped with a 5kN load cell and at of 0.5mmmin−1 crosshead speed according to ISO 6872 [27]. Prior to each measurement, the specimen dimensions were measured by a high precision digital caliper of 0.01mm accuracy.

The average values of flexural modulus of rupture were calculated by Eq. (1) after 5 measurements:

where P is the rupture load in N, l is the test span (center-to-center distance between support rollers) in mm, w is the width of the specimen in mm, and b is the thickness of the specimen in mm.

The samples used in the mechanical tests were pulverized in an agate mortar (D90<100μm), dried at 120°C for 12h and used to determine the density (ρ; gcm−3) using helium pycnometer (Ultrapycnometer 1200e, Quantachrome Instruments, USA). Each density value was the average of five consecutive measurements. The total geometric porosity (TGP; %) was determined by Eq. (2):

where TGP=total geometric porosity (%), Msolid=mass of the solid, L=bar length (cm), W=bar width (cm), T=bar thickness (m) and ρ=solid density (gcm−3).

X-ray diffraction was applied in the 2θ range from 3° to 100° and read at 2° per minute speed by a Rigaku Rotaflex diffractometer, model RV 200B, Japan. The Rietveld refinement [28] method quantified the crystalline phases and the powder that determined the density was also used for X-ray diffraction.

Scanning electron microscopy (SEM) (FEI Inspect F50, Netherlands microscope) was used to determine the morphology of the fracture sections of the samples after the flexural test, as well the morphology of the raw materials. The samples were coated with evaporated carbon using a Q150R Quorum Technologies, UK sputter.

2.2.2Biological tests

Cell culture – Human cells GM07492 (1×103cells/mL) were incubated in a DMEM culture medium supplemented with fetal bovine serum (10vol%) and antibiotics (penicillin 10U/mL; streptomycin 0.1mg/mL). They were incubated at 37±2°C in 5% CO2 atmosphere until reaching 80–90% confluence for seeding the ceramic samples. The GM07492 line is a useful cell line model for studies of adverse cellular effects, as in vitro cytotoxicity, and also as pre-osteoblastic cell in contact with implants in the body.

Cell viability – Cell viability and cell adhesion studies were carried out as the preliminary tests of the mullite biocompatibility. MTT is an indicative test for measuring the mitochondrion dehydrogenase activity (MTT is reduced by NADH to a purple formazan salt). The formazan represents a quantifiable marker for living cells, measured by absorption. For the test the ceramic cylinders were immersed in 24-well plates and the cells (1.5×104cells/mL, 1mL) were seeded on the surface of each cylinder, which were kept at 37±2°C in a 5% CO2 atmosphere for 4h. 2mL of DMEM culture medium was added to each well and the samples remained again under the initial conditions for 72h. The culture medium was withdrawn from the wells; for the MTT test, each cylinder was gently washed with PBS and 2mL of MTT (0.5mg/mL in PBS) were added to each well. The microplates were protected from light and incubated at 37±2°C for 4h in 5% CO2 atmosphere. The cylinders were removed from the wells and washed with PBS. The formazan crystals formed on the surface of the cylinders were solubilized in DMSO (100μL per well) and the absorbance was read at 570nm in an ELISA microplate reader (Polaris-Celer spectrophotometer). The viability assays were performed in triplicate. The DMEM culture medium was used as the negative control and the DMSO solution (25vol% in DMEM) was the positive control. The cell viability was reported in percentage relative to the negative control, calculated using the optical density of the negative control and the optical density of each sample.

Human cell adhesion – The ceramic cylinders were immersed into the wells of 24-well plates. The cells (1.5×104cells/mL, 1mL) were seeded on the surface of each cylinder, and kept in the oven (at 37±2°C and 5% CO2 atmosphere) for 4h. This first step was performed to allow the cells to adhere at the surface of the samples. Then, 2mL of DMEM culture medium were added to each well. The samples were incubated again in the oven (at 37±2°C and 5% CO2 atmosphere) for 72h, to allow the cells grow and proliferate at the surface of the samples. After 72h-incubation, the cells were fixed with glutaraldehyde solution (2.5vol%) for 40min at 8°C, washed with distilled water and dehydrated using increasing ethanol concentration (25, 50, 75 and 100vol%). Their adhesion to the mullite surface was assessed by SEM and fluorescence microscopy. For SEM, the samples were coated with evaporated carbon in a sputter (Q150R Quorum Technologies, UK) and analyzed under a FEI Inspect F50, Netherlands microscope. Optical fluorescence microscopy was carried out under a LeicaDM 750 fluorescence digital microscope. For staining the cells, mullite was immersed into 1μg/mL DAPI solution (10mL) for 10min, washed with PBS and then immersed in 5μg/mL FITC solution (10mL), washed with PBS solution and analyzed by fluorescence microscopy using a green and red filter for DAPI and blue and red filter for FTIC.

The ceramic and all materials used in the experiment were sterilized for 20min in an autoclave at 121°C.

3Results3.1Characterization of the raw materials and mullite

Table 1 shows the results of the characterization of the raw materials regarding typical density, total pore volume, specific surface area, pore diameter and purity. The morphology of microsilica particles assessed by SEM and TEM is shown in Fig. 2, and the images indicate spherical morphology for the particles and an average diameter ranging from 50 to 500nm.

Table 1.

Characteristics of raw materials.

Physico-chemical properties  Microsilicaa  Aluminab  Method and equipment 
Specific surface area (SSA; m2g−124  9.4±0.56c  Nitrogen adsorption using Brunauer-Emmett-Teller method, in a Quantachrome Autosorb 1200e, Quantachrome Instruments, USA
Total pore volume (TPV; cm3g−10.050  2.17±0.33c 
Particle size (D50/D90, μm)  0.086/0.12  0.75/2.9  Particle size distribution (DT-1202, Dispersion Technology Inc., USA) 
Composition (wt%)  SiO2: 94.988Al2O3: 4.242CaO: 0.242SO3: 0.236K2O: 0.196Fe2O3: 0.064ZnO: 0.015MnO: 0.013PdO: 0.003  Al2O3: 99.818Na2O: 0.090Fe2O3: 0.029CaO: 0.044ZnO: 0.007  X-ray dispersive spectroscopy, Shimadzu, EDX 720, Japan 

Microsilica U971, Elkem, Norway.


Alumina, A1000SG; Almatis, USA.


Average value of five measurements and standard deviation.

Fig. 2.

(a) SEM and (b) TEM for commercial silica Microsilica.


The XRD diffraction pattern of mullite is shown in Fig. 3. The main peak that corresponds to mullite (3Al2O3·2SiO2, file JCPDS no. 15-0776) appears at 26°, according to the literature [29]. The reaction of silica with alumina at 1500°C led to the formation of mullite (M peaks), as shown by XRD analysis, Fig. 3. The corundum (C peaks) and cristobalite (S peak) peaks indicate the presence of unreacted starting materials, silica and alumina, respectively. Rietveld refining showed crystalline phases of alumina (corundum: 26.32wt%; 21.59vol%), crystalline silica (cristobalite: 0.046wt%; 0.066vol%) and mullite (73.62wt%; 78.33vol%).

Fig. 3.

X-ray diffraction pattern of mullite obtained at 1500°C. JCPDS file used for identification: C – corundum (JCPDS 42-1468); S – cristobalite (JCPDS 39-1425); M – mullite (JCPDS 15-0776).


The SEM images (Fig. 4) show the morphology of the material treated at 1500°C, which appears as a homogeneous sintered material (Fig. 4a and b), as expected for the solid state reaction with concomitant diffusion of the reagents.

Fig. 4.

Fracture surface of mullite treated at 1500°C.

3.2Mechanical properties and total geometric porosity

Table 2 shows the results of the elastic modulus, flexural strength and total geometric porosity of the samples. The samples treated at 1500°C showed total geometric porosity of 7.8%, which indicates the densification of the material. The densification of the born mullite resulted from the arrangement of the structure at high temperatures at which the particles were sintered and generated the continuous phase. Moreover, the low porosity can be explained by the small dimensions of the particles of the precursor's reagents, which increased the packing and favored the formation of the continuous phase of mullite. The results are in agreement with XRD and SEM and indicate the formation of a dense phase of mullite at 1500°C.

Table 2.

Mechanical properties of mullite.

Materials  Mechanical propertiesReference 
  Elastic modulus (GPa)  Flexural strength (MPa)  Total porosity (%)   
Mullite  135±4.1  109±7.8±0.71  Present study 
Materials for similar applicationsHydroxyapatite[30]
7GPa  48MPa  Not Determined 
Zirconia toughened alumina (ZTA)
289GPa  414MPa  Not Determined 
200GPa  711  Not Determined 
CaP–mullite (20–30wt%)[31]
60–80GPa  75–80  Not Determined 
72GPa  93  Not Determined 
3.3Cell viability (MTT) and cell adhesion on the mullite surface

The cell viability of the negative control was 100% (±0.06) and for the tested sample it was 87.48% (±0.02), indicating no negative effect of the mullite on the cells’ growing capability. According to the international standard ISO 10993-5 [32], a cell viability higher than 70% in comparison to the negative control indicates good biocompatibility.

The images assessed by fluorescence microscopy (Fig. 5) show a large number of cells on the mullite surface and their spread morphology. Fig. 5a displays the blue nuclei of the cells marked with DAPI, thus indicating the high number of cells on the mullite surface. Fig. 5b shows the nuclei marked with DAPI (blue) and the cytoplasm of the cells marked with FITC (green). The spread morphology of the cells (Fig. 5b indicated by arrows) and their confluent monolayer (Fig. 5c), shown by the green cytoskeleton, indicating the cells adhered and proliferated on the mullite surface. The spread morphology of the cells is also an indicative of their viability, in good agreement with the MTT results.

Fig. 5.

SEM of morphology of the cells adhered to the mullite surface.


The spread morphology of an isolated cell assessed by SEM microscopy is shown in Fig. 6a. The isolated cell is fully adhered to the mullite surface. This is confirmed by SEM, as shown in Fig. 6b, whose magnified image indicates the interaction of the cell's (pseudopods) extension anchored to the mullite surface, confirmed by SEM back scattering mode (Fig. 6c and d), where the cells appeared dark and the mullite appears clear. Fig. 6c shows the overall aspect of the sample almost covered by cells (dark area) and Fig. 6d displays the magnification of the cell from Fig. 6c with spread morphology.

Fig. 6.

Images of the fluorescence of the cells adhered to the surface of the mullite sample: (a) nucleus stained with DAPI (blue), (b) spread morphology of the cells and (c) confluence layer of cells on the surface of the mullite and (d) the magnification of a cell from the confluence layer.


The reaction for mullite formation can be affected by parameters, such as particle size of precursors, presence of impurities, heating rate, temperature of thermal processing and nature of the silica source. The latter is one of the main variables that affect the yield, kinetics of the reaction and morphology of the products [33]. The composition of the raw material (Table 1) revealed substances other than silica, such as calcium and potassium, known as liquid phase formers. They improved the formation of viscous mass and increase the wettability of the material, i.e., silica wets alumina, increasing the reactivity of the system for benefiting the formation of mullite [29,34,35]. Regarding morphology, in general, high reactivity is expected for small diameter particles (Fig. 2). The diameter of silica and its amorphous structure are important properties that can favor packing. The small dimension of microsilica tends to accelerate the mullite formation process and to be carried out at low temperatures representing a potential former of mullite phase. The process generates high-density and low-porosity mullite phases. Fig. 4 shows SEM images of mullite fracture; the morphology indicates the formation of a viscous material resulting from the wetting of silica by alumina, favored by the liquid phase sintering, as expected. Such results are in agreement with the XRD data (Fig. 3), which indicate the formation of the mullite phase [34].

The densification of the samples in the sintering process improved their mechanical properties, which is important for biomedical applications, see Table 2. For instance, it is mainly related to loading distribution for bone replacement. In general, the elastic modulus of mullite (Table 2) is higher than the elastic modulus of cortical bones (approximately 20GPa) [36], suggesting its use as potential material for bone replacement. Most ceramic implants are usually developed for hip joint arthroplasty, however there is also a demand for implants of smaller bones that does not demand high mechanical loading, such as radial head in elbow, which could represent an alternative field for the mullite application. The results of cell viability in the presence of mullite are indicative of the biocompatibility of the material, supported by the adhesion studies on their surface, and these results suggest its potential for use in bone replacement.


Mullite was formulated and prepared via sintering reaction by heat treatment at 1500°C, showing low porosity and high density resulting in a material with suitable mechanical properties. Its nature enabled GM07492 cells to survive and proliferate when sown on the surface of the material, as demonstrated by the in vitro cell viability and adhesion tests. The results of the first level of evidence studies (in vitro cytotoxicity tests) showed the absence of cytotoxicity and proliferation of cells at the surface of mullite, which represent an important step for future complementary pre-clinical and clinical studies.

Conflicts of interest

The authors declare no conflicts of interest.


The authors acknowledge CNPq for the PhD grant awarded to L.F. (142372/2014-5), FAPESP (2010/19274-5), CNPq 870346/1997-0, Almatis (Brazil and Germany), Elkem (Norway). They are also indebted Rafael Paiotti M. Guimarães (Evaluation and Interpretation of Rietveld method) and Wagner R. Correr MSc. (Microscopy Laboratory CTMH SMM-EESC/IFSC) for SEM images.

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