Assessment of in vitro bioactivity of SiO2-BaO-ZnO-B2O3-Al2O3 glasses: An optico-analytical approach

Materials Science and Engineering C 32 (2012) 1941–1947

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Assessment of in vitro bioactivity of SiO2-BaO-ZnO-B2O3-Al2O3 glasses: An optico-analytical approach Gurbinder Kaur, Poonam Sharma, Vishal Kumar, K. Singh ⁎ School of Physics & Materials Science, Thapar University, Patiala-147004, India

a r t i c l e

i n f o

Article history: Received 16 August 2011 Received in revised form 12 May 2012 Accepted 22 May 2012 Available online 27 May 2012 Keywords: Bioactive glass Whitlockite Brushite Scanning electron microscopy X-ray diffraction Simulated body fluid

a b s t r a c t Bioactive glasses are an important subclass of biomaterials. The bioactivity of a glass depends on its initial constituents and their respective amounts. In the present investigation, five barium-zinc-borosilicate glass samples have been studied by varying Al2O3 mol% to check their bioactivity. The optical and bioactive properties of pristine glasses are compared with glasses soaked in Simulated Body Fluid (SBF) for 10 and 30 days using pH measurement, Ultraviolet–visible-Near Infrared-red (UV–vis–NIR), Fourier Transform Infra-Red (FTIR) spectroscopy, X-ray diffraction and Scanning Electron Microscopy (SEM) techniques. Although calcium is not present as an initial constituent in glass composition, yet bioactivity is observed in some glass samples after dipping them in SBF. © 2012 Elsevier B.V. All rights reserved.

1. Introduction The biomedical field has been revolutionized by bioceramics due to their advantages over metals and metal based composites. Composites of polymers and ceramics have the tendency to increase the mechanical scaffold stability as well as tissue interaction, but in some cases, ceramic/polymer composites release toxic elements into the human body [1]. Whereas, metal based composites are prone to corrosion-related problems [2,3]. Therefore, glass ceramic can be better bioactive materials due to their good corrosion resistance and better mechanical properties [4]. One of the essential conditions for a glass and glass ceramic, to bond with living bone, is the formation of a bone-like apatite on their surface, when in contact with Simulated Body Fluid (SBF). Kokubo and his colleagues developed an acellular simulated body fluid that has inorganic ion concentrations similar to those of human extra cellular fluid, in order to reproduce the formation of apatite on bioactive materials in vitro. SBF can be used to evaluate bioactivity of artificial materials in vitro. It may also be used as coating fluid on various materials such as glasses under biomimetic conditions [5]. Generally, glasses contain multicomponent oxides that act synergistically to give superior bioactive properties when it comes in contact with SBF. Rehman et al. evaluated the role and impact of one particular subset of biomaterials in tissue engineering applications i.e. bioactive glass for hard and soft-tissue regeneration [6]. Gerhardt [7] has discussed

⁎ Corresponding author. Tel.: + 91 1752393130; fax: + 91 1752393005. E-mail address: [email protected] (K. Singh). 0928-4931/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.msec.2012.05.034

porous bone tissue engineering scaffolds on the basis of melt-derived bioactive silicate glasses and their composite structures. Many bioglass contain significant amount of alkali oxides such as Na2O or K2O. 45S5 is the most commonly used bioglass for many biomedical applications due to its high healing capability, but at the same time, it exhibits high dissolution rate due to large alkali content [8,9]. The presence of alkali increases thermal expansion coefficient as well as water uptake by osmosis [10]. Some bioactive glass compositions developed over the years contain additional elements incorporated in the silicate network such as boron [11,12], aluminum [13] and zinc [14,15]. It has been reported by Manupriya et al. [16] that borate glasses have faster dissolution rate and lower chemical durability as compared to silicate glasses in xCaO- (1− x) B2O3 system. In our earlier work [17,18], the structural and sealing properties of SiO2-BaO-ZnO- xB2O3- (10 − x) Al2O3 have been investigated. The replacement of B2O3 by Al2O3 increases the thermal as well as chemical stability of these glasses. Therefore, it is worthwhile to study the effect of Al2O3 on bioactivity in alkali free glasses. In our present work, an attempt has been made for in vitro studies on apatite layer formation in SiO2-BaO-ZnO-xB2O3- (10 − x) Al2O3 glasses (0≤ x ≤ 10). Many researchers have reported zinc aluminosilicate glasses to be the chemical durable material with good mechanical properties [19]. Zinc oxide is a bacteriocide which can act as network modifier or intermediate oxide in a fashion similar to alumina [20]. Additionally, zinc ions are also being used for de-oxyribonucleic acid (DNA) replication as well as stimulator for protein synthesis [21]. Alumina has high hardness and abrasive resistance which is associated with surface smoothness and surface energy of the ceramic [22]. Oxides of barium increase the surface adherence by reducing surface tension [23]. Basically, it is a very strong glass modifier enhancing non-bridging oxygen

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(NBO's) in glass structure which may enhance the formation of apatite layer. Barium crystals are also used as an opacifier in bone cements [24–26]. The main aim is to understand the mechanism behind bioactivity as a function of physical and chemical characteristics of the glass and its structural correlation with apatite layer formation. Analysis of optical spectra is one of the most beneficial tools to understand the electronic structure of amorphous materials as this technique gives idea about the change on the surface of the glasses [26,13]. Therefore, the bioactive and optical properties of pristine glasses as well as glasses soaked in SBF for 10 and 30 days were investigated using pH measurement, Ultraviolet–visible-Near Infra-red (UV–vis–NIR), Fourier Transform Infra-Red (FTIR) spectroscopy, X-ray diffraction (XRD) and scanning electron microscopy (SEM) techniques.

Glass samples were sliced into uniform rectangular pieces using diamond cutter. All the slices were of almost similar dimension and approximately same weight of 1000 mg. These glass slices were then dipped in SBF solution for different time durations. The SBF solution was prepared using the required ion concentrations [4,29]. The pH was measured using a Mettler–Toledo pH meter (TMP-85), SBF was adjusted to pH 7.25 at 36.5 °C, by using 50 mM (=mmol/dm3) of tris (hydroxymethyl) aminomethane and approximately 45 mM of HCl. When apatite-forming ability of the specimen is not so high, pH of SBF is sometimes adjusted to pH 7.40. 3. Results and discussion 3.1. pH measurement

2. Experimental procedure

n 3 2
hv  Eopt 5 αhv ¼ const ¼ 4 hv

ð1Þ

where hν is photon energy, n = 1/2 and Eopt is direct optical band gap. Eopt values are obtained by extrapolating (αhν)2 = 0 for the curves (αhν)2 as a function of photon energy hν. Fourier Transform Infra-Red (FTIR) spectra were recorded at room temperature in the region 500–2000 cm − 1 using Perkin Elmer Spectrum BX (2) spectrometer. The spectral resolution of FTIR spectroscopy was ±1 cm − 1. 5 mg of each sample was mixed with 20 mg of KBr in an agate mortar and then this powder was used for recording the transmission spectra. The spectrum of each sample was normalized to the spectrum of the blank KBr. The scanning electron microscopy (SEM) and Electron Dispersive Spectroscopy (EDS) were done using ZEISS (EVO 10) to study the surface morphology of phase formed and analysis of its chemical composition, respectively.

The hydrolytical stability of all the glasses in SBF was evaluated by pH measurements. The data obtained from pH measurement of SBF at different time durations has been presented in Fig. 1. It does not show any appreciable change in pH during the experiment. However, Hench [29] has reported that the formation of hydroxyapatite (HAP) depends upon pH of SBF. Hydroxyapatite is a naturally occurring mineral and a prominent component of vertebrate bone as well as tooth enamel having stoichiometry of Ca10(PO4)6(OH)2 [29]. The increase in pH in aqueous environment is due to dissolution of ions such as Ca 2+, Na +, PO43−, and Si 4+ from the glass [2,29,30]. However, in the present glass compositions, only Si 4+ cations are present which may be the reason for less change in the pH values during durability measurement. 3.2. XRD analysis The XRD spectra for all the as prepared glasses BZA (I), BZA (II), BZA (III), BZA (IV), and BZA (V) possess the characteristic amorphous hump. A representative X-ray diffraction pattern of BZA (V) sample, before and after dipping in SBF solution for 10 days is given in Fig. 2(a), to indicate the absence of sharp crystalline peaks in both diffractograms. It clearly indicates that the amorphous state of glass has not changed even after dipping it in SBF for 10 days. The XRD pattern of all the glasses soaked for 30 days is given in Fig. 2(b). As the time duration for dipping increases from 10 to 30 days, nucleation of crystalline phases takes place in case of BZA (IV) and BZA (V) samples. The new crystalline phases are 7.8

B Z A (V )

7.6 7.4 7.8

B Z A (IV )

7.6 7.4 B Z A ( III)

7.8

pH

The glass compositions, chosen for the present study, are listed in Table 1. The glasses were prepared by taking required stoichiometric amounts of different constituent oxides or carbonates of high purity (99.9%). These constituents were first mixed together using ball-mill in acetone medium. The powder obtained after ball-milling was melted at 1550 °C in high resistance furnace. The melt was quenched in air using copper plates. The quenched glass was then annealed at 500 °C to remove the internal stress from the glasses. The XRD pattern of glasses was recorded using a PANalytical Xperts Pro. MPD diffractometer with Cu Kα radiations. The pattern was recorded at a scanning rate of 2°min− 1 with angular range of 10–60°. The optical transmission spectra of the glasses were recorded at room temperature using a double beam UV–vis–NIR spectrophotometer (Model: Perkin Elmer 55) in the wavelength range of 200–1200 nm. Glass powder was prepared by grinding glass in agate mortar and pestle. The glass powder was dissolved in methanol for UV–vis–NIR experiments. The spectrum of each sample was normalized to the spectrum of the blank methanol. Furthermore, the band gap of samples (before and after dipping) was calculated in Tauc's region [27], corresponding to high absorption. Mott and Davis [28] discussed absorption coefficient in Tauc's region using following quadratic form:

7.6 7.4 7.8

B Z A ( II)

7.6 7.4 7.8

Table 1 Composition of glass samples along with their labels in mol%.

B Z A ( I)

7.6 Sample name

SiO2

BaO

ZnO

B2O3

Al2O3

BZA BZA BZA BZA BZA

40 40 40 40 40

30 30 30 30 30

20 20 20 20 20

10 7.5 5 2.5 0

0 2.5 5 7.5 10

(I) (II) (III) (IV) (V)

7.4 0

300

TIME (hrs) Fig. 1. Variation of pH of SBF with time.

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type of large metal sites [33]. TCP is the most important biodegradable ceramic material because it contains the property of osteosynthesis along with cell proliferation [34]. The thermodynamic solubility (Ksp) of brushite and whitlockite phase is −6.59 and −81.7, respectively indicating less solubility of whitlockite [35]. When an oxide of a trivalent element (M2O3) is introduced in a silicate structure, MO4 structural units are formed substituting the SiO4 ones (act as network former) or the cations can be allocated in the holes of structure as ‘network modifying ion’ [36]. Moreover, McMillan [37] found that the network modifier cation should have ionic field strength Z/r 2 b 5 Å− 2, where Z is cation valence state and r is the radius of ion. If the value of Z/r2 is greater than 5 Å− 2, then the cation acts as glass former. As Al 3+ is having Z/r2 ≈ 11.53 Å − 2 [38], hence it may enter as a network forming cation. For the substitution of Al2O3, AlO4 tetrahedron is obtained and Al3+ is believed to occupy its center. The addition of Al2O3, in such cases produces 1.5 oxygen per network forming cation. The formation of whitlockite and brushite layer on the surface of present glasses, especially in Al2O3 contained glasses can be proposed as follows: (a) When the bioactive glass is in contact with the physiological solution, then the process of layer formation on the surface starts with an ionic exchange between the glass and the solution. (b) Loss of silica occurs forming silanol groups Si(OH)4 which acts as catalyst to nucleate apatite layer [39]. The hydrolysis reaction can be given as: Si    O    Si þ H2 O→2Si    OH

ð2Þ

(c) The precipitation and migration of calcium ions from the supersaturated solution onto the surface of ceramics occur followed by the incorporation of OH−/PO42− anions from the solution to form a mixed hydroxyl phosphate layer.

Fig. 2. (a) XRD spectra of BZA (V) before and after dipping in SBF solution for 10 days. (b) XRD spectra of all the samples after dipping in SBF solution for 30 days.

identified as whitlockite (Ca3 (PO4)2) and brushite (CaHPO4·2H2O) using JCPDS card no. 0620426 and 021351 respectively. For whitlockite the peaks appeared at 2θ ≈29.55°, 34.46°, 43.69°, 45.3°, 50.07°, 53.21°, 56.402°, 59.59° and 63.38° whereas the peak position for brushite phase are at 2θ≈34.32°, 43.69°, 51.28°, 57.55° and 59.59°. BZA (IV) glass sample exhibits only whitlockite phase. On the other hand, BZA (V) glass sample contains brushite phase in addition to whitlockite. BZA (V) exhibits more prominent and sharp peaks of whitlockite in comparison to BZA (IV) sample. At the same time, BZA (I), BZA (II) and BZA (III) could not demonstrate any detectable peak in XRD pattern indicating absence of crystalline layer on the surface of these glasses. CaHPO4·2H2O (CHP) is one of the most soluble calcium phosphate phases and clinically it is used as a minor powder component in calcium phosphate cements designed for skeletal and dental repair [31]. CHP has triclinic unit cell with a = 6.910, b = 6.627 and c = 6.998 Å, respectively. Its structure consists of CaHPO4 chains held together by Ca\O bonds and three types of hydrogen bonds [32]. Ca3 (PO4)2 (TCP) have lattice parameters a = 10.4 and c = 37.4 Å, where a phosphorus atom is tetrahedral coordinated by oxygen atoms and calcium occupy two

Al2O3 behaves as network modifier, as its concentration increases above 5 mol% and hence it increases the bioactivity [40]. Many researchers have reported that the addition of network formers in glass reduces the bioactivity as they tend to decrease the basicity of silanol group which hinders the substitutions [41]. On the other hand, the addition of network modifier (>5 mol%) enhance the bioactivity due to more open structure along with higher basicity. Therefore, BZA (IV) and BZA(V) samples exhibit the presence of whitlockite and brushite/whitlockite layers respectively as the alumina plays the role of network modifier in these glasses. Additionally, the presence of ZnO and Al2O3 may also encourage the formation of BO4 units in the present glasses. The presence of BO4 units might have prevented/ delayed the formation of hydroxyapatite layer on glass surface [16]. 3.3. Energy band gap measurement The process of layer formation involves a set of reactions like dissolution, precipitation and ion exchange between glass and SBF [29]. Obviously, some compositional changes in glass must have taken place during ion exchange process leading to change in their optical properties. Hence band gap measurements can give an idea about the changes occurring in the glasses and their surfaces. Band gap is a region where a particle or quasiparticle is forbidden from propagating. Near the absorption edge of UV–visible spectra, two types of transitions take place namely direct and indirect [28]. Direct band gap means direct combination of electrons at conduction band minimum with holes at valence band maximum while conserving momentum. Indirect band gap means recombination of an electron and hole with the mediation of third body such as phonon or a crystallographic defect which allows conservation of momentum. The values of Eopt are listed in Table 2. In addition to this, Fig. 3 shows band gap of BZA (V) sample before and after dipping for 10 days and 30 days in SBF solution. The obtained results give further

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(a)

Table 2 Band gap of glasses before and after dipping in SBF solution. Sample label

Band gap before dipping in SBF(eV)

Band gap after dipping in SBF for 10 days (eV)

Band gap after dipping in SBF for 30 days (eV)

BZA(I) BZA(II) BZA(III) BZA(IV) BZA(V)

4.98 5.22 5.46 5.71 5.85

4.86 5.14 5.37 4.38 4.79

4.71 4.97 5.29 3.83 3.62

(b) 130

-

Si-O streching B-O vibrations Si-O-Si streching

125

BZA(V)

120

Fig. 3. Band gap of unsoaked, 10 days and 30 days SBF soaked BZA (V) sample.

insight of the of whitlockite and brushite layer formation. In other words, the band gap may change, if a layer formation takes place on the surface of the sample due to the reaction between SBF solution and glass samples after dipping. It can be observed from Table 2 that the band gap increases from 4.9 eV to 5.6 eV with increasing content of Al2O3. Its introduction will cause the conversion of non‐bridging oxygen (NBO) to bridging oxygen (BO) and hence top of valence band gets subside resulting in higher energy gap [42]. After dipping, BZA (IV) and BZA (V) glasses show sharp decrement in the band gap. Basically the change in optical band gap is attributed to the structural changes due to the different site occupancies by cations. The XRD of 30 days soaked BZA (IV) and BZA (V) glasses show the formation of crystalline layers on the surface of the glasses which reduce the porosity of glass samples and increase the ordering leading to decrease in optical band gap [13]. The optical band gap of soaked and unsoaked BZA (I), BZA (II) and BZA (III) have not shown remarkable difference indicating absence of whitlockite or brushite layer on their surface which is also supported by X-ray diffractograms for these samples. It indicates during 30 days soaking, some dissolution might have taken place in early stage of soaking. 3.4. Fourier transform infrared spectroscopy The infrared absorption spectra of the glasses have been recorded in order to obtain information about the possible changes of vibration spectra due to the process of structural rearrangement with a change in glass composition. Fig. 4(a), (b) and (c) shows the FTIR spectra of samples before and after the immersion in the simulated body fluid for 10 and 30 days. Fig. 4. (a) Fourier transform-infrared (FTIR) absorption spectra of samples before dipping in SBF solution. (b) Fourier transform-infrared (FTIR) absorption spectra of samples after dipping in the SBF solution for 10 days. (c) Fourier transform-infrared (FTIR) absorption spectra of samples after dipping in the SBF solution for 30 days.

Transmittance

BZA(IV)

115 BZA(III)

110 105

BZA(II)

100 BZA(I)

95 90 500

1000

1500

Wavenumber (cm-1)

(c)

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Fig. 5. Typical SEM micrographs of unsoaked (a) BZA (IV) and (b) BZA (V) glass samples.

In the region from 574 to 940 cm − 1 small kinks are also observed nearly about 568–650 cm − 1 which can be due to Si\O − stretching with two non bridging oxygen and other kinks observed at 770– 902 cm − 1 which is due to the Si\O\Si symmetric stretching of bridging oxygen between tetrahedral [43,44]. The transmittance bands in the region 1350–1550 cm − 1 corresponds to B\O vibrations in the BO triangle [45,46]. These bands get shifted under the influence of surrounding cations, the extent and the direction of the shift depends upon the chemical nature of cations. FTIR spectra of the glasses show that in these glasses boron primarily occurs in the form of BO3 triangles. However, the presence of BO4 tetrahedron in the glass structure cannot be neglected. A band is also observed at 1000 cm − 1 which belongs to BO4 tetrahedron [47]. The FTIR spectra of 30 days soaked BZA (IV) and BZA (V) glasses show appearance of the new bands. In BZA (IV), band appearing in the range 1075–1126 cm− 1 corresponds to the P\O vibrations, indicating the initiation of deposition of PO42− ions [48]. For BZA (V) sample, three bands appear at 520–525 cm− 1, 1075–1126 cm− 1 and 1280– 1299 cm− 1. Band at 520–525 cm− 1 can be attributed to HO\PO3 bending mode whereas 1280–1299 cm− 1 corresponds to P\OH bending modes originating from HPO4 groups [49]. These results indicate that deposition/formation of whitlockite and brushite layer has taken place in case of BZA (IV) and BZA (V) glass samples. Fig. 6. SEM micrograph of (a) BZA (I) (b) BZA (II) and (c) BZA (III) samples after soaking in SBF for 30 days.

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Fig. 7. SEM micrograph of BZA (IV) sample after 30 days soaking in SBF indicating globular layer formation on the glass surface.

Fig. 8. (a) SEM micrographs of BZA (V) sample after 30 days soaking in SBF showing flakes as well as globules on the surface of glass and (b) EDS of whitlockite phase.

G. Kaur et al. / Materials Science and Engineering C 32 (2012) 1941–1947

3.5. SEM analysis Fig. 5(a–b) shows the typical micrographs of unsoaked BZA (IV) and BZA (V) pristine glasses. These glasses exhibit smooth topography. The micrographs of BZA (I), BZA (II) and BZA (III) samples after dipping them for 30 days in SBF shows heterogeneous surface as seen from Fig. 6. For BZA (IV) samples, a layer of spherical particles covering the glass surface could be seen as shown in Fig. 7. These spheres have grown in BZA (V) sample with higher densification as compared to the BZA (IV) sample which is visible clearly in Fig. 8(a). As compared to pristine glass samples (Fig. 5(a–b)), the soaked BZA (IV) and BZA (V) glass samples show some remarkable changes in the microstructure as shown in Figs. 7 and 8(a–b). Apart from this, in BZA (V) sample, flake-like structure is also present on the surface along with the globular crystals. The EDS analysis (Fig. 8(b)) of spheres confirms the presence of calcium and phosphorus which are the constituents of whitlockite. The flake-like structure can be brushite phase which have appeared in BZA (V) sample. The results obtained are in agreement with XRD, FTIR and UV–vis–NIR spectra of these samples. 4. Conclusion BZA (IV) and BZA (V) glasses show the formation of whitlockite and brushite/whitlockite layers, respectively during in vitro test. On the other hand, BZA (I), BZA (II) and BZA (III) glasses could not form CaHPO4·2H2O /Ca3(PO4)2 layer on the glass surface where B2O3/Al2O3 ratio is higher. BZA (IV) and BZA (V) have shown the formation of whitlockite and brushite phases after they were soaked in SBF for 30 days. These phases are useful for bioactive applications. The band gap decreases drastically particularly in soaked BZA (IV) and BZA (V) samples. FTIR spectra of soaked BZA (IV) and BZA (V) show the presence of HO-PO3 and P\OH bands due to HPO4 group which further enhances the growth of whitlockite and brushite layers. Acknowledgment The authors are thankful to Dr. O. P. Pandey, Professor (SPMS), Thapar University for his expert advice. The authors are also thankful to Ms. Anu Arora, Mr. Ravi Shukla and Mr. Dinesh, Thapar University for their help during the spectral recording. One of the authors (GK) is thankful to DST (SR/WOS-A/PS-23/2009), New Delhi for the financial assistance. References [1] T.V. Thamaraiselvi, S. Rajeswari, Trends Biomater. Artif. Organs 18 (2004) 9–17. [2] K. Rezwan, Q.Z. Chen, J.J. Blaker, Aldo Roberto Boccaccini, Biomaterials 27 (2006) 3413–3431. [3] V.A. Dubok, Powder Metall. Met. Ceram. 39 (2000) 381–394. [4] J.C. Bokras, L.D. Lagrange, F.J. Schoen, Chem. Phys. Carbon 9 (1992) 104–169. [5] T. Kokubo, S. Ito, S. Sakka, T. Yamamuro, J. Mater. Sci. 21 (1986) 536–540.

1947

[6] M.N. Rahaman, D.E. Day, B.S. Bal, Q. Fu, S.B. Jung, L.F. Bonewald, A.P. Tomsia, Acta Biomater. 7 (2011) 2355–2373. [7] L.C. Gerhardt, A.R. Boccaccini, Materials 3 (2010) 3867–3910. [8] D. Zhang, M. Hupa, L. Hupa, Acta Biomater. 5 (2008) 1498–1505. [9] Q.-Z. Chen, Y. Li, L.-Y. Jin, J.M.W. Quinn, P.A. Komesaroff, Acta Biomater. 6 (2010) 4143–4145. [10] A. Goel, S. Kapoor, R.R. Rajagopal, M.J. Pascual, H.-W. Kim, J.M.F. Ferreira, Acta Biomater. 8 (2012) 361–372. [11] X. Liu, W. Huang, H. Fu, A. Yao, D. Wang, H. Pan, W. Lu, X. Jiang, X. Zhang, J. Mater. Sci. Mater. Med. 20 (2009) 1237–1243. [12] M.F. Gorriti, J.M. Porto Lopez, A.R. Boccaccini, C. Audisio, A.A. Gorustovich, Adv. Eng. Mater. 11 (2009) B67–B70. [13] K. Singh, I. Bala, V. Kumar, Ceram. Int. 35 (2009) 3401–3406. [14] V. Aina, G. Malavasi, A. Fiorio Pla, L. Munaron, C. Morterra, Acta Biomater. 5 (2009) 1211–1222. [15] S. Haimi, G. Gorianc, L. Moimas, B. Lindroos, H. Huhtala, S. Raty, H. Kuokkanen, G.K. Sandor, C. Schmid, S. Miettinen, R. Suuronen, Acta Biomater. 5 (2009) 3122–3131. [16] Manupriya, K.S. Thind, K. Singh, V. Kumar, G. Sharma, D.P. Singh, D. Singh, J. Phys. Chem. Solids 70 (2009) 1137–1141. [17] A. Arora, A. Goel, E.R. Shabaan, K. Singh, O.P. Pandey, J.M.F. Ferreira, Physica B 403 (2008) 1738–1746. [18] A. Arora, K. Singh, O.P. Pandey, Int. J. Hydrogen Energy 36 (2011) 14948–14955. [19] G. Lusvardi, G. Malavasi, L. Menabue, M.C. Menziani, J. Phys. Chem. B 106 (2002) 9753–9760. [20] A. Rosenthal, S.H. Garoflaini, J. Am. Ceram. Soc. 70 (1987) 821–826. [21] M. Yamaguchi, T. Matsui, Peptides 17 (1996) 1207–1211. [22] S. Kannan, A. Balamurgan, S. Rajeswari, M. Subaiyyan, Corrosion Rev. 20 (2002) 339–358. [23] K.S. Weil, JOM 58 (2006) 37–44. [24] R. Madanat, N. Moritz, E. Vedel, E. Svedstro, H.T. Aro, Acta Biomater. 5 (2009) 3497–3505. [25] G. Lewis, C.S. van Hooy-Corstjens, A. Bhattaram, L.H. Koole, J. Biomed. Mater. Res. B 73 (2005) 77–87. [26] D.T. Pierce, W.E. Spicer, Phys. Rev. B 5 (1972) 3017–3029. [27] J. Tauc, Amorphous and Liquid Semiconductors, London, , 1974. [28] N.F. Mott, E.A. Davis, Electronic Processes in Non-Crystalline Materials, Clarendon, Oxford, 1979. [29] L.L. Hench, CRC Handbook of bioactive glasses and glass ceramics, CRC Press, Boca Raton, 1990. [30] L.L. Hench, J. Mater. Sci. Mater. Med. 17 (2006) 967–978. [31] R.J. Martin, P.W. Brown, J. Cryst. Growth 183 (1998) 417–426. [32] L. Tortet, J.R. Gavarri, G. Nihoul, A.J. Dianoux, J. Solid State Chem. 132 (1997) 6–16. [33] K. Sugiyama, M. Tokonami, Phys. Chem. Miner. 15 (1986) 125–134. [34] C. Tardei, F. Grigore, I. Pasuk, S. Stoleriu, J. Optoelectron. Adv. Mater. 8 (2006) 568–571. [35] F.C.M. Driessens, R.M.H. Verbeck, Biominerals, CRC Press, Boca Raton, 1990. [36] H. Rawson, Inorganic Glass Forming System, Academic Press, London, 1967. [37] P.W. Mcmillan, Glass Ceramics, Academic Press, London, 1964. [38] R.C. Weast, CRC Handbook of Chemistry and Physics, CRC Press, Ohio, 1977. [39] T. Kokubo, J. Non-Cryst. Solids 120 (1990) 138–151. [40] N. Lahl, K. Singh, L. Singheiser, K. Hilpert, J. Mater. Sci. 35 (2000) 3089–3096. [41] F. Branda, F. Arcobello-Varlese, A. Costantini, G. Luciani, Biomaterials 23 (2002) 711–716. [42] J.A. Duffy, Phys. Chem. Glasses 42 (2001) 151. [43] M. Bosca, L. Pop, G. Borodi, P. Pascuta, E. Culea, J. Phys. Conf. Ser. 182 (2009) 012061. [44] H.A. Elbatal, M.I. Khalil, N. Nada, S.A. Desouky, Mater. Chem. Phys. 82 (2003) 375–387. [45] S. Simon, I. Ardelean, S. Filip, I. Bratu, I. Cosma, Solid State Commun. 116 (2000) 83–86. [46] E.G. Parada, P. Gonzalez, J. Pou, J. Serra, D. Fernandez, B. Leon, M. Perez-Amor, J. Vac. Sci. Technol. A14 (1996) 436–440. [47] Z.A. ElHadi, M.A. ElBaki, Phys. Chem. Glasses 40 (1999) 40–48. [48] H. Moore, H. Winkelmann, J. Soc. Glass Technol. 39 (1959) 215–218. [49] S. Mandel, A.C. Tas, Mater. Sci. Eng., C 30 (2010) 245–254.