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. 2016 Mar;50(1):40–48. doi: 10.15644/asc50/1/6

Titanium Ions Release from an Innovative Titanium-Magnesium Composite: an in Vitro Study

Zlatko Stanec 1,✉, Jasna Halambek 2, Krešimir Maldini 3, Martin Balog 4, Peter Križik 4, Zdravko Schauperl 5, Amir Ćatić 6
PMCID: PMC5017277  PMID: 27688425

Abstract

Background

The innovative titanium-magnesium composite (Ti-Mg) was produced by powder metallurgy (P/M) method and is characterized in terms of corrosion behavior.

Material and methods

Two groups of experimental material, 1 mass% (Ti-1Mg) and 2 mass% (Ti-2Mg) of magnesium in titanium matrix, were tested and compared to commercially pure titanium (CP Ti). Immersion test and chemical analysis of four solutions: artificial saliva; artificial saliva pH 4; artificial saliva with fluoride and Hank balanced salt solution were performed after 42 days of immersion, using inductively coupled plasma mass spectrometry (ICP-MS) to detect the amount of released titanium ions (Ti). SEM and EDS analysis were used for surface characterization.

Results

The difference between the results from different test solutions was assessed by ANOVA and Newman-Keuls test at p<0.05. The influence of predictor variables was found by multiple regression analysis. The results of the present study revealed a low corrosion rate of titanium from the experimental Ti-Mg group. Up to 46 and 23 times lower dissolution of Ti from Ti-1Mg and Ti-2Mg, respectively was observed compared to the control group. Among the tested solutions, artificial saliva with fluorides exhibited the highest corrosion effect on all specimens tested. SEM micrographs showed preserved dual phase surface structure and EDS analysis suggested a favorable surface bioactivity.

Conclusion

In conclusion, Ti-Mg produced by P/M as a material with better corrosion properties when compared to CP Ti is suggested.

Key words: Titanium; Magnesium; Corrosion; Immersion; Saliva, Artificial; Ion Exchange

Introduction

Despite long-standing use of titanium as a biomaterial of good biocompatibility (1), there is a certain number of papers in recent scientific literature reporting its undesirable corrosion properties (2-4). The main corrosion characteristic of titanium is the passivation i.e. the formation of a highly protective passive dioxide layer (5) that protects the metal from further corrosion. However, such a protective surface layer shows poor protective function in low pH value conditions (3, 6) and in the presence of fluoride (F) (7, 8). The low pH value is typical of inflammatory condition (9) that may correspond to the condition of surgical wound immediately after implantation (10). Also, low pH value may be found in the oral cavity with a large amount of biofilm and high metabolic activity of cariogenic bacteria (11, 12). Fluoride is ubiquitous in oral hygiene products such as toothpastes and mouthwashes.

The consequence of the titanium biomaterial corrosion is the release of titanium ions (Ti) in the surrounding area. Mine et al. have shown on the cell culture that Ti could interfere with the process of differentiation of osteoblasts and osteoclasts and adversely affect the whole process of healing and osseointegration (13). Similarly, the experiments made by Wachi et al., on the animal model, suggested that accumulated Ti in the surrounding connective and gingival tissue might induce the infiltration of monocytes, the production of cytokines and consequently, the differentiation of osteoclast cells that could lead to clinically significant alveolar bone resorption (14). The study of Barao et al. showed that the corroded surface more easily accumulated the pathogenic bacteria that could lead to inflammatory changes around the implant (15). Due to long-term application of titanium-based dental implants, the problem of hypersensitivity and allergy to titanium which could provoke dental implant failure is emphasized. Although some clinical trials on the topic of titanium allergy have already been carried out (16), most authors agree with the fact that so far there are still not enough data on such complications and that, for better understanding, it is necessary to have more evidence-based data and to perform more detailed longitudinal clinical studies (2, 17).

Magnesium has recently been in the focus of scientific interest due to its favorable effect on the process of osseointegration (18-20). As the essential macro element of the human body, Mg participates in important intracellular energy processes (21) and stimulates the differentiation of pluripotent cells, proliferation and migration of osteoblasts (22). Galli et al. demonstrated that the presence of Mg promoted gene expression of osteogenic markers and improved osteoconduction (23). Castellani et al., in an animal model, showed that Mg obtained greater contact surface of the implant-bone interface and better mechanical strength without the occurrence of systemic inflammatory response in contrast to titanium (24). However, due to its biodegradable properties, high chemical reactivity and unfavorable corrosion behavior, pure Mg as a dental biomaterial can be used only in combination with other metallic biomaterials (25).

Powder metallurgy (P/M) is a technological approach used for titanium-based biomaterials processing in order, among other things, to improve the mechanical properties of materials and to reduce the price of the production process (26). Adverse effects of long-term applied titanium biomaterials (27, 28) produced by conventional ways point to the need for a new strategy in the production of biomaterials. P/M can be a way to improve not only mechanical properties and to reduce the costs but also to achieve such a biological response that can be denominated as biomimetic (29, 30). The procedure of P/M consists of mixing metal powders, homogenization, compacting and consolidation through a suitable technological process and finally sintering to bond powder particles (31). In the present study, titanium-magnesium composite (Ti-Mg) was prepared by mixing powders of titanium matrix with 1 and 2 mass% of magnesium (Mg).

A possible technical solution for improvement of corrosion resistance of Ti-based biomaterials is introduction of an alternative production technology i.e. powder metallurgy. The aim of the present study was to explore the corrosion behavior of an innovative Ti-Mg material and to compare it to commercially pure titanium (CP Ti). Test solutions were used to simulate biological environment (e.g., mouth, bone). It is assumed that the amount of Mg in the titanium matrix significantly affects the corrosion behavior of tested material. Fluoride and low pH value of the surrounding media are hypothesized as significantly corrosive environmental factors for the material in question.

Materials and methods

Materials preparation

Materials used in this research (Ti-1Mg and Ti-2Mg) were produced by means of P/M technology. The 99.4% α-titanium powder produced by hydrid-dehydrid (HDH) technology, with the median particle size of <150 μm, was mixed with 1 or 2 mass% of atomized 99.8% Mg powder, with the median particle size of 30 μm, respectively. Blending of powder mixtures was performed for 30 min using Turbula mixer, GlenMills, Clifton, USA. After the homogenization of powders, the loose powder mixtures were cold compacted by cold isostatic pressing (CIP) at 200 MPa. CIP powder billets were compressed by uniaxial vacuum pressing (VP) at 500 şC and 1300 MPa in fully consolidated sound Ti-Mg composite materials. Commercially pure titanium grade 4 for biomedical use (CP Ti 4), Acnis International, France, produced by conventional process of casting and hot rolling was used for the control group of specimens in the as-received form of a bar. The samples were divided into two groups: test group containing specimens of Ti-1Mg and Ti-2Mg; and the control group containing CP Ti 4. All materials were then cut using the wire electrical discharge machining (wire EDM) technique. Twelve specimens of each material were prepared in the discs shape with the 27 mm diameter and 4 mm thickness. The specimen surfaces were prepared using standard metallographic methods, ground and polished using wet silicon-carbide paper (according to ISO 6344-1) from #320 - 4000 successively, on a grinder/polisher Phoenix Alpha, Buehler, USA, at 60 rpm.

Test solutions

In this study, four testing solutions for immersion of specimens were used:

a) Modified Fusayama’s artificial saliva (AS) (contained 0.4 g of NaCl, 0.4 g of KCl, 0.795 g of CaCl2 ∙ 2H2O, 0.69 g of NaH2PO4 ∙ 2H2O, 0.005 g of Na2S ∙ 9H2O and 1.0 g urea in 1000 ml of deionized water); b) Modified Fusayama’s artificial saliva-pH 4 prepared by adding lactic acid (C3H6O3) to AS and adjusting the pH value to 4; c) Modified Fusayama’s artificial saliva with F prepared by adding 0.2 mass% sodium fluoride (NaF) to AS; d) Hank’s balanced salt solution (HBSS) (contained 8.0 g of NaCl, 1.0 g of d-glucose, 0.4 g of KCl, 0.35 g of NaHCO3, 0.14 g of CaCl2, 0.098 g of MgSO4 ∙ 7H2O, 0.06 g of KH2PO4, 0.048 g of Na2HPO4 in 1000 ml deionized water). All chemicals were of analytical grade. According to the ISO 3696 deionized water used in this research was grade 2. All solutions were prepared freshly prior to the immersion.

Static immersion test

The static immersion test was carried out in accordance with the currently specified standard for corrosion test of metallic materials in dentistry ISO 10271:2011. Surface area (in cm2) of each specimen was measured using a micrometer gauge at the start of the experiment. The specimens were cleaned ultrasonically for 2 minutes in ethanol, rinsed with deionized water and dried with oil- and water-free compressed air (according to the standard ISO 7183) prior to immersion. The samples were set in triplicates for each material and each type of solution. Each specimen was placed in its individual volumetric flask made of borosilicate glass (according to the standard ISO 1042), using metal-free pincers, immersed in freshly prepared solution such that it did not touch the flask surface except in a minimum support line and that it was completely covered by the solution. In additional parallel sets, the flasks of blank tests in triplicates without samples were set and these were treated in identical manner. pH value and volume of each test solution were measured before and after immersion period using pH-meter HQ440d Multi-Parameter Meter, Hach, USA. All flasks were closed to prevent evaporation. The experiment was performed at 37 şC in thermostat. The immersion was carried out for 42 days. After the period of immersion, the specimens were taken out, rinsed with deionized water and gently dried. Test solutions were taken and transferred in polypropylene tubes for chemical analysis.

The mass concentration of dissolved Ti (μg/l) was measured using inductively coupled plasma mass spectrometry (ICP-MS) on mass spectrometer Elan 9000, Perkin-Elmer, USA with automatic sampler Perkin-Elmer AS 93plus, Perkin-Elmer, USA, in three replicates, under following conditions: nebulizer gas flow rate 0.9 l/min, ICP-RF power 1000 W, lens voltage 7.75 V, analog stage voltage -1887 V, pulse stage voltage 1100 V, discriminator threshold 65 V and AC rod offset -2.9 V. Series of calibration solutions were prepared to determine the mass concentration of dissolved Ti using standard Perkin-Elmer Pure Plus Multi-Elemental Calibration Standard 5, Perkin-Elmer, USA.

The amount of Ti released for each specimen (μg/cm2) was calculated from the data of the mass concentration in test solutions, blank test and surface area using formula: the amount of released Ti (μg/cm2) = volume of test solution (l) ∙ (mass concentration of Ti in test solution (μg/l) - mean mass concentration of Ti in blank test with three flasks (μg/l)) / surface area of specimen (cm2). The quantity of dissolved Ti is considered zero at the Ti concentration below that of the blank test. The mean quantity and standard deviation were calculated for the three flasks.

Surface analysis

Specimen surface analysis was performed by means of scanning electron microscope (SEM) type VEGA TS5136LS, Tescan, Czech Republic, using SE and BSE detectors at a magnification of 50 and 200 times with electron beam acceleration voltage of 20 kV. Chemical microanalysis of the surface was performed by energy-dispersive spectroscopy (EDS) using the EDS detector, Oxford Instruments, UK. Inca software, Oxford Instruments, UK, was used to process the EDS data.

Statistical analysis

Statistical evaluation was performed by Statistica, Dell Software, USA, software package. Mean values and standard deviations for the amount of released Ti were calculated by basic statistic method. For the assessment of the differences in the amount of dissolved Ti among three materials tested and four different solutions, the analysis of variance (ANOVA) and Newman-Keuls test were used. The influence of the test solution and type of material on the amount of Ti released from the material was determined by multiple regression analysis and General regression model. A p<0.05 was taken to indicate statistical significance.

Results

Amount of released Ti

In the case of experimental Ti-1Mg and Ti-2Mg, there was no significant difference in the amount of the released Ti ions among the test solutions. In HBSS Ti-1Mg and Ti-2Mg, the tests showed the result of 0.32 ± 0.05 μg/cm2 and 0.32 ± 0.07 μg/cm2, respectively. Significant difference can be observed in AS, AS-pH 4 and AS with F: 0.02 ± 0.03 μg/cm2 vs. 0.04 ± 0.05 μg/cm2, 0.09 ± 0.13 μg/cm2 vs. 0.00 ± 0.00 μg/cm2 and 0.67 ± 0.01 μg/cm2 vs. 0.48 ± 0.09 μg/cm2, respectively. However, the difference between the amount of dissolved Ti in AS with F and HBSS was evident. In the case of CP Ti 4, AS and HBSS exhibited similar corrosive ability and the amount of released Ti reached 0.93 ± 0.01 μg/cm2. Only a slightly higher Ti releasing was observed at pH 4 (1.63 ± 0.01 μg/cm2). The dissolving of Ti increased more than 11 times in the presence of F ions and the amount reached 10.80 ± 0.01 μg/cm2. Figure 1 demonstrates the comparison of the amount of the released Ti among three tested materials in four different solutions.

Figure 1.

Figure 1

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Comparison of the amount of the released Ti among three tested materials in four different test solutions: AS - artificial saliva; AS pH-4 - artificial saliva-pH 4; AS with F - artificial saliva with fluoride; HBSS - Hank’s balanced salt solution after 42 days of immersion

Analysis of variance (ANOVA) (Table 1) showed statistically significant difference in the amount of released Ti among test solutions for three tested materials (Ti-1Mg: p=0.002574; Ti-2Mg: p=0.004284; CP Ti 4: p=0.000000). Newman-Keuls test revealed that in the case of Ti-1Mg there was statistically significant difference in the amount of released Ti between AS with F and all other solutions (AS pH 4 vs. AS with fluoride p=0.002792). Similarly, in the case of Ti-2Mg there was statistically significant difference between AS and AS with F (p=0.001590). The results of multiple regression analysis (Table 2) showed good, statistically significant correlation (R=0.68; p<0.01766) between predictor variables (test solution, material) and the amount of released Ti. According to beta coefficients, only the type of the test solution had statistically significant influence on the Ti dissolution (p=0.006078).

Table 1. Results of ANOVA testing for the amount of released Ti from tested materials (Ti-1Mg, Ti-2Mg, CP Ti 4) in different solutions.

material SS Effect df Effect MS Effect SS Error df Error MS Error F p
Ti-1Mg 0.5 3 0.2 0.020 4 0.0050 34.4 0.002574*
Ti-2Mg 0.3 3 0.1 0.020 4 0.0040 26.3 0.004284*
CP Ti 4 209.93 3 69.98 0.00 8 0.00 699756.75 0.000000*
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* significantly different at p<0.05

Table 2. Results of multiple regression analysis testing for correlation between predictor variables and the amount of released Ti.

Predictor
variable 		Statistical parameter
Beta p
Solution 0.67 0.006078*
Alloy 0.14 0.496139
R=0.68; p<0.01766*
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*significantly different at p<0.05

Surface analysis

SEM micrographs with BSE detector of Ti-1Mg, Ti-2Mg and CP Ti 4, as shown in Figure 2, demonstrated preserved heterogeneous dual phase surface structure of test specimens after 42 day immersion with discreetly formed corrosion products. EDS analysis of corrosion precipitates on the surface of the specimen immersed in HBSS (Figure 3) showed that they were mainly composed of atoms of Ti and O or Ca, P and O. On the other hand, precipitates formed on test specimens immersed in the AS with fluorides (Figure 4) using EDS analysis, demonstrated the presence of Mg and F.

Figure 2.

Figure 2

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SEM micrographs of test (a) Ti-1Mg, (b) Ti-2Mg and (c) control CP Ti 4 at magnification of 50 times using BSE detector after 42 day immersion in artificial saliva with fluorides.

Figure 3.

Figure 3

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Micrographs and EDS analysis of corrosion products on the surface of test specimen containing a) Ti and O, b) Ca, P and O mainly, after 42 day immersion in HBSS.

Figure 4.

Figure 4

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EDS analysis of corrosion products on the surface of test a) Ti-1Mg and b) Ti-2Mg specimen after 42 day immersion in the artificial saliva with fluorides, containing Mg and F atoms mainly.

Discussion

Commercially pure titanium, widely used in clinical dental medicine, shows very poor corrosion resistance in the condition of low pH and the presence of F. However, only the addition of F in AS increases the amount of released Ti ions for one order of magnitude that is consistent with a presumption of F as a very aggressive and reactive halogen that can destroy the protective dioxide film. Similarly, Milošev et al. in an in vitro study demonstrated a high rate of titanium corrosion in the presence of F after 32 days of immersion (7). Study of Sartori et al. (32), performed on dental implants made from CP Ti 4, treated with F and used only SEM and EDS method, showed that there was no evidence of corrosion on the specimens surfaces. In contrast, the present study demonstrated that there were no signs of corrosion observed using SEM analysis, there was a high amount of released Ti from the surface of CP Ti 4 in the presence of fluoride. This can lead to the conclusion that SEM observation is not a sufficient method to assess the corrosion behavior especially if the corrosion is presented in a generalized form without the appearance of pits or crevices.

When compared to CP Ti 4, the experimental Ti-1Mg and Ti-2Mg demonstrate similar tendency in respect of the amount of dissolved Ti ions among four different test solutions. The highest value and statistically significant difference were observed in AS with F. The addition of new components to titanium matrix can be the strategy to improve the corrosion behavior of a new material and achieve better biocompatibility. Rosalbino et al., in an electrochemical study, demonstrated better corrosion resistance of studied material produced by adding noble metals to titanium (33). Fojt et al., in the study with Ti-39Nb alloy, reported that the process of powder metallurgy and consequent porosity could be the reason for better corrosion resistance of such materials (34).

Moreover, the presence of magnesium and micro-galvanic corrosion effect may lead to improved corrosion behavior of tested material in the present study. Galvanic corrosion occurs when two dissimilar metals are in physical and electrical contact in an aqueous solution. The dual phase structure of Ti-Mg material and direct inter-metallic contact between titanium and Mg components could cause the more electronegative metal as anode, which is in this case Mg, to protect the other one (titanium) as cathode from the corrosion, i.e., dissolving. Additionally, magnesium aggravates forming insoluble magnesium hydroxide (Mg(OH)2), which in fluoridated solution turns into magnesium fluoride (MgF2), also a highly insoluble layer that protects the surface from further corrosion. In HBSS, high concentration of chloride ions distorts the passive layer of Mg(OH)2 by forming magnesium chloride (MgCl2) which is soluble. The result is increased dissolution of Mg. Such a reaction could promote the passivation of titanium by forming a titanium-oxide (TiO2) and deposing a hydroxyapatite (HA) layer. Similarly, Jung et al. reported improved nucleation and growth of HA crystals in the presence of Mg (35). The same mechanism may favor bioactivity in titanium-magnesium experimental material.

However, further research is needed for a better understanding of the chemical and biological properties, surface characteristics and potential bioactivity of this material.

Conclusion

The following conclusions were reached:

  1. Reported results confirm low release of Ti from innovative experimental material. Up to 46- and 23- fold lower amount of dissolved Ti from Ti-1Mg and Ti-2Mg, respectively was observed when compared to control CP Ti.

  2. The corrosion behavior is highly dependent on the type of test solution. Among the tested solutions, AS with F exhibited the highest corrosion effect on all three materials tested.

  3. Mg content in the range of 1 and 2 mass% had no significant influence on corrosion behavior of the two tested experimental materials.

From the above mentioned, one can conclude that the Ti-1Mg and Ti-2Mg materials have high corrosion resistance. The static immersion test performed by using chemical models (test solutions) which can mimic the real biological environment only partially, could be a limitation of the present study. However, possible wider application of tested materials in dental medicine is suggested.

Footnotes

The authors deny any conflict of interest

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