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Electrical activity of ferroelectric biomaterials and its effects on the adhesion, growth and enzymatic activity of human osteoblast-like cells
This content has been downloaded from IOPscience. Please scroll down to see the full text. 2016 J. Phys. D: Appl. Phys. 49 175403 (http://iopscience.iop.org/0022-3727/49/17/175403) View the table of contents for this issue, or go to the journal homepage for more
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Journal of Physics D: Applied Physics J. Phys. D: Appl. Phys. 49 (2016) 175403 (12pp)
doi:10.1088/0022-3727/49/17/175403
Electrical activity of ferroelectric biomaterials and its effects on the adhesion, growth and enzymatic activity of human osteoblast-like cells P Vaněk1, Z Kolská2, T Luxbacher3, J A L García4, M Lehocký4, M Vandrovcová5, L Bačáková5 and J Petzelt1 1
Institute of Physics of the Czech Academy of Sciences, Na Slovance 2, CZ-18221 Prague, Czech Republic 2 Faculty of Science, J. E. Purkyně University, České mládeže 8, CZ-40096 Ústí nad Labem, Czech Republic 3 Anton Paar GmbH, Anton Paar Str. 20, A-8054 Graz, Austria 4 Centre of Polymer Systems, Tomáš Baťa University in Zlín, nám T G Masaryka 5555, CZ-76001 Zlín, Czech Republic 5 Institute of Physiology of the Czech Academy of Sciences, Vídeňská 1083, CZ-14220 Prague, Czech Republic E-mail:
[email protected] Received 21 December 2015, revised 2 March 2016 Accepted for publication 11 March 2016 Published 1 April 2016 Abstract
Ferroelectrics have been, among others, studied as electroactive implant materials. Previous investigations have indicated that such implants induce improved bone formation. If a ferroelectric is immersed in a liquid, an electric double layer and a diffusion layer are formed at the interface. This is decisive for protein adsorption and bioactive behaviour, particularly for the adhesion and growth of cells. The charge distribution can be characterized, in a simplified way, by the zeta potential. We measured the zeta potential in dependence on the surface polarity on poled ferroelectric single crystalline LiNbO3 plates. Both our results and recent results of colloidal probe microscopy indicate that the charge distribution at the surface can be influenced by the surface polarity of ferroelectrics under certain ‘ideal’ conditions (low ionic strength, non-contaminated surface, very low roughness). However, suggested ferroelectric coatings on the surface of implants are far from ideal: they are rough, polycrystalline, and the body fluid is complex and has high ionic strength. In real cases, it can therefore be expected that there is rather low influence of the sign of the surface polarity on the electric diffusion layer and thus on the specific adsorption of proteins. This is supported by our results from studies of the adhesion, growth and the activity of alkaline phosphatase of human osteoblastlike Saos-2 cells on ferroelectric LiNbO3 plates in vitro. Keywords: biomaterials, ferroelectric, zeta potential, osteoblast-like cells (Some figures may appear in colour only in the online journal)
0022-3727/16/175403+12$33.00
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© 2016 IOP Publishing Ltd Printed in the UK
P Vaněk et al
J. Phys. D: Appl. Phys. 49 (2016) 175403
1. Introduction
It follows from previous studies that the use of electricallyactive ceramics on the surface of implants can bring benefits compared to existing implant materials. Among electrically active materials, ferroelectrics can be advantageous due to their spontaneous polarization and simultaneous piezo electricity. However, previous studies have not taken into account the fact that the charge at the surface is always quickly compensated (screened) by the opposite charge from the surroundings. Kalinin et al [16, 17] showed that the charge at the surface of polarized BaTiO3 (or the ferroelectric domain) is fully screened at room temperature by the adsorbed charges from the air, so that the charge on the surface is opposite to the charge from the polarization. If a ferroelectric is immersed in a liquid (e.g. tissue fluid), it is obvious that an electric double layer and a diffusion layer are formed on its surface. To the best of our knowledge, there have been no studies about the charge distribution in such a case, except for one recent paper [18]. It was therefore not clear how the spontaneous polarization in ferroelectrics affects the charge distribution in a liquid at the surface of ferroelectrics, and therefore the adsorption of proteins. Ferris et al [18] found by colloidal probe force microscopy that the ion distribution within the double layer in a dilute electrolyte at an ultrasmooth ferroelectric PZT film can be changed by reversing the ferroelectric polarization. If a ferroelectric is exposed to dynamically changing stress (loading), its surface charge is influenced by the piezoelectric effect, and this can additionally affect the charge distribution in the liquid, and also the behaviour of cells in contact with the material. The charge distribution at the spontaneously polarized ferroelectrics immersed in a liquid can also be characterized, in a simplified way, by the zeta potential (the potential at the ‘slipping’ plane). The zeta potential and its dependence on pH have frequently been measured on colloidal ferroelectric BaTiO3 particles, because the zeta potential is crucial for the stability of colloidal suspensions. However, the dependence of the zeta potential on the polarity of the surface of poled ferroelectrics has not been investigated until now. Our paper will report on measurements of this type, together with their correlation with the adhesion, growth and the activity of alkaline phosphatase (ALP) of human bone-derived cells on ferroelectric surfaces. To avoid possible side effects (e.g. grain boundaries, roughness), poled well-polished single crystalline ferroelectric plates with polarization perpendicular to the surface were considered for the measurements. Two materials were taken into account—BaTiO3 and LiNbO3. BaTiO3 is known to be biocompatible, but it has lower stability of the polarization, and Ba2+ ions are transiently leached from the surface to an adjacent liquid [19]. LiNbO3 has good stability of polarization (spontaneous polarization 71 μC cm−2, coercive field 21 kV mm−1, Curie temperature 1160 °C) and it is also chemically stable. Recent studies have shown that LiNbO3 and other related ceramics (e.g. LiTaO3 or lithium sodium potassium niobate) are biocompatible, i.e. promoting the adhesion, growth and other functions of osteoblasts and fibroblasts in cultures on these materials [20–23]. LiNbO3 and LiTaO3 ceramics are also bioactive, i.e. promoting the formation
Biomaterials, i.e. natural or artificial materials designed for application in biotechnologies and in medicine, are widely used for replacing irreversibly damaged tissues in the human body. Bone implants, e.g. hip and teeth implants, are frequently applied, but efforts are still being made to improve the healing and the biocompatibility of the implant material. It is well known that bones are electrically active under mechanical loading, due to the piezoelectricity of collagen [1, 2], the possible ferroelectricity of nanocrystalline hydroxyapatite [3], and the flow of ionic fluids within the bone structure (streaming potential) [4]. The electrical potential in mechanically loaded bone has been linked to the mechanical adaptation of the bone in response to loading [5–7], leading to the suggestion that the addition of an electrically active component (e.g. a coating) to an implant material may improve healing and integration with the surrounding living tissue. Recently, interest has grown in exploiting this phenomenon to develop electrically active ceramics for implantation in hard tissue, which may induce improved biological responses [8]. Both polarized hydroxyapatite, the surface charge of which is not dependent on loading, and piezoelectric ceramics, which produce electrical potentials under stress, have been studied in order to determine the possible benefits of using electrically active bioceramics as implant materials. The polarization of hydroxyapatite has a positive influence on interfacial responses to the ceramic [8, 9]. In vivo studies of polarized hydroxyapatite have shown polarized samples to induce improvements in bone ingrowth [8, 10]. Most of the piezoelectric ceramics proposed for implant use contain barium titanate (BaTiO3). In vivo and in vitro investigations have indicated that ceramics of this kind are biocompatible and, under appropriate mechanical loading, induce improved bone formation around implants [8]. The mechanism by which the electrical activity has a positive influence on biological responses is not yet clearly understood, but it is likely to result from preferential adsorption of proteins and ions on to the polarized surface. However, a detailed examination of the literature shows that the results of the studies mentioned above are somewhat ambiguous. For hydroxyapatite, the growth of osteoblasts during in vitro tests depends not only on the surface electric charge, but also on the surface roughness and topology [10]. The tests in vivo are sometimes ambiguous, and can differ from the tests in vitro [9]. In most studies, cell growth is favoured by a negative charge on the surface, but some tests have shown that a positive charge is preferred [8]. The (+) surface charge formed by NH+ 3 groups on the surface of plasma-treated fluorinated polymers grafted by cysteamine lead to improved cytocompatibility [11]. For ferroelectric (i.e. also piezoelectric) BaTiO3 and its composites, BaTiO3–polyvinylidenfluoride– trifluorethylene [12], TiO2–BaTiO3 [13] and hydroxyapatite– BaTiO3 [14, 15], the results are also somewhat ambiguous. In most of these materials, a negative charge on the surface is preferred for cell growth. Most experiments on piezoelectrics have been done without loading, or with insufficiently controlled loading. 2
P Vaněk et al
J. Phys. D: Appl. Phys. 49 (2016) 175403
Figure 1. Scheme of the adjustable gap cell. The electrolyte flows alternately from left to right and back from right to left.
of apatite-like structures on their surface when immersed into simulated body fluid [24]. However, both LiNbO3 and LiTaO3, tested in the form of microparticle powder, were transiently releasing Li+ ions. Lithium is a well-known mood stabilizer clinically applied for treatment of psychiatric dis orders. Studies in vitro revealed than in lower doses, lithium acted as cytoprotective, antiapoptotic and preventing the oxidative damage of different type of cells [25–27]. However, at higher doses Li showed opposite effects, i.e. it acted cytotoxically, antimitotically, pro-apoptotically and caused oxidative damage of cells [26, 27]. It can be expected that the release of higher concentrations of Li+ ions is more likely in LiNbO3 in the form of powder than in the form of films or bulk material [24]. As for niobium, it has been considered as a promising non-toxic component of novel beta-titanium alloys (e.g. TiNb), intended to replace potentially toxic aluminum or vanadium present in TiAlV alloys, which are used in current clinical practice as orthopaedic and dental implants [28, 29]. Another important parameter for choosing the material was the price, single crystalline BaTiO3 plates are much more expensive than LiNbO3 plates. Regarding all relevant parameters, LiNbO3 was chosen as a model material for our measurements.
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