Laminin Coating Promotes Calcium Phosphate Precipitation on Titanium Discs in vitro
Identifieur interne : 000694 ( Pmc/Corpus ); précédent : 000693; suivant : 000695Laminin Coating Promotes Calcium Phosphate Precipitation on Titanium Discs in vitro
Auteurs : Kostas Bougas ; Victoria Franke Stenport ; Fredrik Currie ; Ann WennerbergSource :
- Journal of Oral & Maxillofacial Research [ 2029-283X ] ; 2012.
Abstract
The objective of this study was to investigate the effect of a laminin coating on calcium phosphate precipitation on three potentially bioactive titanium surfaces in simulated body fluid.
Blasted titanium discs were prepared by alkali and heat treatment (AH), anodic oxidation (AO) or hydroxyapatite coating (HA) and subsequently coated with laminin. A laminin coated blasted surface (B) served as a positive control while a blasted non coated (B-) served as a negative control. Surface morphology was examined by Scanning Electron Microscopy (SEM). The analysis of the precipitated calcium and phosphorous was performed by Energy Dispersive X-ray Spectroscopy (EDX).
The thickness of the laminin coating was estimated at 26 Å by ellipsometry. Interferometry revealed that the coating process did not affect any of the tested topographical parameters on µm level when comparing B to B-. After 2 weeks of incubation in SBF, the alkali-heat treated discs displayed the highest calcium phosphate deposition and the B group showed higher levels of calcium phosphate than the B- group.
Our results suggest that laminin may have the potential to be used as a
coating agent in order to enhance the osseoinductive performance of
biomaterial surfaces, with the protein molecules possibly functioning as
nucleation centres for apatite formation. Nevertheless,
Url:
DOI: 10.5037/jomr.2011.2405
PubMed: 24422002
PubMed Central: 3886082
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PMC:3886082Le document en format XML
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<author><name sortKey="Bougas, Kostas" sort="Bougas, Kostas" uniqKey="Bougas K" first="Kostas" last="Bougas">Kostas Bougas</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Prosthodontics, Faculty of Odontology, Malmö University</institution>
<addr-line>Malmö</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff4"><institution>Department of Biomaterials, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Stenport, Victoria Franke" sort="Stenport, Victoria Franke" uniqKey="Stenport V" first="Victoria Franke" last="Stenport">Victoria Franke Stenport</name>
<affiliation><nlm:aff id="aff2"><institution>Department of Prosthodontics, Faculty of Odontology, Sahlgrenska Academy, University of Gothenburg</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff4"><institution>Department of Biomaterials, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Currie, Fredrik" sort="Currie, Fredrik" uniqKey="Currie F" first="Fredrik" last="Currie">Fredrik Currie</name>
<affiliation><nlm:aff id="aff3"><institution>Promimic AB</institution>
<addr-line>Gothenburg</addr-line>
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<author><name sortKey="Wennerberg, Ann" sort="Wennerberg, Ann" uniqKey="Wennerberg A" first="Ann" last="Wennerberg">Ann Wennerberg</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Prosthodontics, Faculty of Odontology, Malmö University</institution>
<addr-line>Malmö</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff4"><institution>Department of Biomaterials, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Laminin Coating Promotes Calcium Phosphate Precipitation on Titanium Discs <italic>in vitro</italic>
</title>
<author><name sortKey="Bougas, Kostas" sort="Bougas, Kostas" uniqKey="Bougas K" first="Kostas" last="Bougas">Kostas Bougas</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Prosthodontics, Faculty of Odontology, Malmö University</institution>
<addr-line>Malmö</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff4"><institution>Department of Biomaterials, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Stenport, Victoria Franke" sort="Stenport, Victoria Franke" uniqKey="Stenport V" first="Victoria Franke" last="Stenport">Victoria Franke Stenport</name>
<affiliation><nlm:aff id="aff2"><institution>Department of Prosthodontics, Faculty of Odontology, Sahlgrenska Academy, University of Gothenburg</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff4"><institution>Department of Biomaterials, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Currie, Fredrik" sort="Currie, Fredrik" uniqKey="Currie F" first="Fredrik" last="Currie">Fredrik Currie</name>
<affiliation><nlm:aff id="aff3"><institution>Promimic AB</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Wennerberg, Ann" sort="Wennerberg, Ann" uniqKey="Wennerberg A" first="Ann" last="Wennerberg">Ann Wennerberg</name>
<affiliation><nlm:aff id="aff1"><institution>Department of Prosthodontics, Faculty of Odontology, Malmö University</institution>
<addr-line>Malmö</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff4"><institution>Department of Biomaterials, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</nlm:aff>
</affiliation>
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<series><title level="j">Journal of Oral & Maxillofacial Research</title>
<idno type="eISSN">2029-283X</idno>
<imprint><date when="2012">2012</date>
</imprint>
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<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<sec sec-type="objectives"><title>Objectives</title>
<p>The objective of this study was to investigate the effect of a laminin
coating on calcium phosphate precipitation on three potentially bioactive
titanium surfaces in simulated body fluid. </p>
</sec>
<sec sec-type="material and methods"><title>Material and Methods</title>
<p>Blasted titanium discs were prepared by alkali and heat treatment (AH),
anodic oxidation (AO) or hydroxyapatite coating (HA) and subsequently coated
with laminin. A laminin coated blasted surface (B) served as a positive
control while a blasted non coated (B-) served as a negative control.
Surface morphology was examined by Scanning Electron Microscopy (SEM). The
analysis of the precipitated calcium and phosphorous was performed by Energy
Dispersive X-ray Spectroscopy (EDX).</p>
</sec>
<sec sec-type="results"><title>Results</title>
<p>The thickness of the laminin coating was estimated at 26 Å by ellipsometry.
Interferometry revealed that the coating process did not affect any of the
tested topographical parameters on µm level when comparing B to B-. After 2
weeks of incubation in SBF, the alkali-heat treated discs displayed the
highest calcium phosphate deposition and the B group showed higher levels of
calcium phosphate than the B- group.</p>
</sec>
<sec sec-type="conclusions"><title>Conclusions</title>
<p>Our results suggest that laminin may have the potential to be used as a
coating agent in order to enhance the osseoinductive performance of
biomaterial surfaces, with the protein molecules possibly functioning as
nucleation centres for apatite formation. Nevertheless, <italic>in vivo</italic>
studies are
required in order to clarify the longevity of the coating and its
performance in the complex biological environment.</p>
</sec>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Oral Maxillofac Res</journal-id>
<journal-id journal-id-type="iso-abbrev">J Oral Maxillofac Res</journal-id>
<journal-id journal-id-type="publisher-id">JORM</journal-id>
<journal-title-group><journal-title>Journal of Oral & Maxillofacial Research</journal-title>
</journal-title-group>
<issn pub-type="epub">2029-283X</issn>
<publisher><publisher-name>Stilus Optimus</publisher-name>
<publisher-loc>Kaunas, Lithuania</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24422002</article-id>
<article-id pub-id-type="pmc">3886082</article-id>
<article-id pub-id-type="publisher-id">v2n4e5ht</article-id>
<article-id pub-id-type="doi">10.5037/jomr.2011.2405</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Original Paper</subject>
</subj-group>
</article-categories>
<title-group><article-title>Laminin Coating Promotes Calcium Phosphate Precipitation on Titanium Discs <italic>in vitro</italic>
</article-title>
</title-group>
<contrib-group><contrib id="contrib1" contrib-type="author" corresp="yes"><name><surname>Bougas</surname>
<given-names>Kostas</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
<contrib id="contrib2" contrib-type="author"><name><surname>Stenport</surname>
<given-names>Victoria Franke</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
<contrib id="contrib3" contrib-type="author"><name><surname>Currie</surname>
<given-names>Fredrik</given-names>
</name>
<xref ref-type="aff" rid="aff3">3</xref>
</contrib>
<contrib id="contrib4" contrib-type="author"><name><surname>Wennerberg</surname>
<given-names>Ann</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
</contrib-group>
<aff id="aff1" rid="aff1"><sup>1</sup>
<institution>Department of Prosthodontics, Faculty of Odontology, Malmö University</institution>
<addr-line>Malmö</addr-line>
<country>Sweden.</country>
</aff>
<aff id="aff2" rid="aff2"><sup>2</sup>
<institution>Department of Prosthodontics, Faculty of Odontology, Sahlgrenska Academy, University of Gothenburg</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</aff>
<aff id="aff3" rid="aff3"><sup>3</sup>
<institution>Promimic AB</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</aff>
<aff id="aff4" rid="aff4"><sup>4</sup>
<institution>Department of Biomaterials, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg</institution>
<addr-line>Gothenburg</addr-line>
<country>Sweden.</country>
</aff>
<author-notes><corresp>Kostas Bougas,
<institution>Department of Prosthodontics, Faculty of Odontology, Malmö
University</institution>
<addr-line>205 06 Malmö</addr-line>
<country>Sweden</country>
<phone>+46 40 6658520</phone>
Fax: +46 40 6658503<email>kostas.bougas@mah.se</email>
</corresp>
</author-notes>
<pub-date pub-type="collection"><season>Oct-Dec</season>
<year>2011</year>
</pub-date>
<pub-date pub-type="epub"><day>1</day>
<month>1</month>
<year>2012</year>
</pub-date>
<volume>2</volume>
<issue>4</issue>
<elocation-id>e5</elocation-id>
<history><date date-type="received"><day>25</day>
<month>8</month>
<year>2011</year>
</date>
<date date-type="accepted"><day>16</day>
<month>9</month>
<year>2011</year>
</date>
</history>
<permissions><copyright-statement> Copyright © Bougas K, Stenport VF, Tengvall P, Currie F,
Wennerberg A. Published in the JOURNAL OF ORAL &
MAXILLOFACIAL RESEARCH (http://www.ejomr.org), 1 January 2012.</copyright-statement>
<copyright-year>2011</copyright-year>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/"><license-p>This is an open-access article, first published in the JOURNAL OF
ORAL & MAXILLOFACIAL RESEARCH, distributed under the terms of the
Creative Commons Attribution-Noncommercial-No Derivative Works 3.0 Unported
License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/">http://creativecommons.org/licenses/by-nc-nd/3.0/</ext-link>
), which permits unrestricted non-commercial use, distribution, and
reproduction in any medium, provided the original work and is properly
cited. The copyright, license information and link to the original
publication on <ext-link ext-link-type="uri" xlink:href="http://www.ejomr.org">http://www.ejomr.org</ext-link>
must be included.</license-p>
</license>
</permissions>
<self-uri xlink:type="simple" xlink:href="http://www.ejomr.org/JOMR/archives/2011/4/e5/v2n4e5ht.htm"></self-uri>
<abstract><title>ABSTRACT</title>
<sec sec-type="objectives"><title>Objectives</title>
<p>The objective of this study was to investigate the effect of a laminin
coating on calcium phosphate precipitation on three potentially bioactive
titanium surfaces in simulated body fluid. </p>
</sec>
<sec sec-type="material and methods"><title>Material and Methods</title>
<p>Blasted titanium discs were prepared by alkali and heat treatment (AH),
anodic oxidation (AO) or hydroxyapatite coating (HA) and subsequently coated
with laminin. A laminin coated blasted surface (B) served as a positive
control while a blasted non coated (B-) served as a negative control.
Surface morphology was examined by Scanning Electron Microscopy (SEM). The
analysis of the precipitated calcium and phosphorous was performed by Energy
Dispersive X-ray Spectroscopy (EDX).</p>
</sec>
<sec sec-type="results"><title>Results</title>
<p>The thickness of the laminin coating was estimated at 26 Å by ellipsometry.
Interferometry revealed that the coating process did not affect any of the
tested topographical parameters on µm level when comparing B to B-. After 2
weeks of incubation in SBF, the alkali-heat treated discs displayed the
highest calcium phosphate deposition and the B group showed higher levels of
calcium phosphate than the B- group.</p>
</sec>
<sec sec-type="conclusions"><title>Conclusions</title>
<p>Our results suggest that laminin may have the potential to be used as a
coating agent in order to enhance the osseoinductive performance of
biomaterial surfaces, with the protein molecules possibly functioning as
nucleation centres for apatite formation. Nevertheless, <italic>in vivo</italic>
studies are
required in order to clarify the longevity of the coating and its
performance in the complex biological environment.</p>
</sec>
</abstract>
<kwd-group><kwd>laminin</kwd>
<kwd>titanium</kwd>
<kwd>biomaterials</kwd>
<kwd>calcium phosphates</kwd>
<kwd>dental implants</kwd>
<kwd>osseointegration.</kwd>
</kwd-group>
</article-meta>
</front>
<body><sec><title>INTRODUCTION</title>
<p>Bone anchored titanium implants are widely used in the rehabilitation of edentulism.
In order to enhance bone growth around implants, various chemical modifications of
titanium surfaces have been proposed. Some techniques are alkali-heat treatment (AH)
[<xref ref-type="bibr" rid="B1">1</xref>
], anodization [<xref ref-type="bibr" rid="B2">2</xref>
], coatings of calcium phosphates in sol-gels [<xref ref-type="bibr" rid="B3">3</xref>
] and immobilization of organic bio-molecules
on the surface [<xref ref-type="bibr" rid="B4">4</xref>
].</p>
<p>The simulated body fluid (SBF) model has been extensively utilized for <italic>in vitro</italic>
evaluation of various materials and surface modification methods [<xref ref-type="bibr" rid="B5">5</xref>
-<xref ref-type="bibr" rid="B7">7</xref>
]. The
SBF is defined as a solution with ion concentrations approximately equal to those of
human blood plasma [<xref ref-type="bibr" rid="B8">8</xref>
-<xref ref-type="bibr" rid="B10">10</xref>
]. The nucleating capacity of a biomaterial can be observed
by immersing it in SBF [<xref ref-type="bibr" rid="B11">11</xref>
]. It has been
suggested that the nucleation of calcium/phosphates from SBF, mimics the initial
mineralization of bone on the implant surface. The correlation between apatite
formation in SBF models and bone bioactivity <italic>in vivo</italic>
has been described in a review
on the usefulness of SBF in predicting <italic>in vivo</italic>
bone bioactivity [<xref ref-type="bibr" rid="B12">12</xref>
]. However, compared to the SBF model, the <italic>in
vivo</italic>
process is much more complex and proteins, enzymes and biological factors play
a crucial role in this process [<xref ref-type="bibr" rid="B13">13</xref>
].</p>
<p>Laminin is an organic biomolecule previously utilized with success for improving the
attachment of mesenchymal stem cells on TiO<sub>2</sub>
nanotubes [<xref ref-type="bibr" rid="B14">14</xref>
] and for enhancing the epithelial cell attachment on
Ti-6Al-4V implants <italic>in vitro</italic>
[<xref ref-type="bibr" rid="B15">15</xref>
,<xref ref-type="bibr" rid="B16">16</xref>
]. Laminins are heterotrimeric glycoprotein
molecules that bind to a protein family known as integrins, especially β1 and
β2 integrins [<xref ref-type="bibr" rid="B17">17</xref>
]. Integrins are
integral membrane glycoproteins which mediate cell-to-cell and cell-to-matrix
interactions. Integrins are known to mediate cell adhesion to extracellular matrix
and to facilitate the cell communication [<xref ref-type="bibr" rid="B18">18</xref>
]. One of their key functions is to participate in the assembly of the
cytoskeleton and thereby resulting in cell migration, adhesion of epithelial cells
and hemidesmosome formation by their cytoplasmic domains [<xref ref-type="bibr" rid="B17">17</xref>
]. <italic>In vitro</italic>
studies indicate that laminin-1 selectively
recruits osteoprogenitors through an integrin β1-dependent cell attachment
effect [<xref ref-type="bibr" rid="B19">19</xref>
,<xref ref-type="bibr" rid="B20">20</xref>
] and possesses the ability to stimulate osteoblasts to produce
alkaline phosphatase and deposit mineral [<xref ref-type="bibr" rid="B21">21</xref>
]. Our hypothesis is that by coating titanium surfaces with laminin-1
enhanced precipitation of CaP in an SBF model may be achieved. </p>
<p>The aim of the present study was to investigate the effects of laminin coating on
titanium surfaces modified by three methods claimed to provide bioactivity in terms
of Ca/P precipitation, surface morphology and surface chemistry in simulated body
fluid.</p>
</sec>
<sec sec-type="materials|methods"><title>MATERIAL AND METHODS</title>
<p><bold>Surface preparations</bold>
</p>
<p>Ninety discs (diameter = 8 mm, thickness = 1 mm) of titanium grade 4 were included in
the study. The samples were blasted with Al<sub>2</sub>
O<sub>3</sub>
powder with an average particle size
of 120 µm with a force of 3.5 kg and from a distance of 15 mm and subsequently
ultrasonically cleaned in diluted Extran MA01 and absolute ethanol and dried at 60
°C for 24 h. The specimens were then divided into five equally sized groups (n =
18). One group of blasted discs was coated with laminin and served as a positive
control (B), while a non laminin-coated group of blasted specimens served as a
negative control (B-). The other three groups were treated as follow and were
ultimately coated with laminin.</p>
<p>Alkali and heat treatment (AH)</p>
<p>Alkali and heat treatment was performed as described in the literature [<xref ref-type="bibr" rid="B10">10</xref>
,<xref ref-type="bibr" rid="B22">22</xref>
,<xref ref-type="bibr" rid="B23">23</xref>
]. In brief, the discs were
soaked in 5 M aqueous NaOH for 24 h at 60 °C, rinsed with distilled water and dried
at 40 °C for 24 h. Subsequently, the discs were heated until reaching 600 °C by
increasing the temperature by 5 °C/min in an electrical furnace (Bitatherm, Bita
Laboratory Furnaces, Israel) and were kept at 600 °C for 2 h. At the end of the
process, the discs were left in the furnace until they cooled down to room
temperature.</p>
<p>Anodic oxidation (AO)</p>
<p>The samples were prepared in a mixed electrolyte containing calcium ions by the Micro
Arc Oxidation (MAO) method in a galvanostatic mode as described in the literature
[<xref ref-type="bibr" rid="B24">24</xref>
]. More specifically, the
electrochemical cell was composed of platinum plates as cathodes with a titanium
anode at the centre. A computer interfaced with a DC power supply was used to record
currents and voltages at milliseconds intervals. The content of ripple was
controlled to less than 0.1% [<xref ref-type="bibr" rid="B25">25</xref>
]. Surface
analysis of the oxidizedsurfaces demonstrated the following properties: a calcium
content of 11 atomic percent in the newly formed oxide of 1.2 µm thickness, 24%
porosity and mixed anatase and rutile crystal structure [<xref ref-type="bibr" rid="B26">26</xref>
,<xref ref-type="bibr" rid="B27">27</xref>
].</p>
<p>Hydroxyapatite coating (HA)</p>
<p>A thin hydroxyapatite layer (< 50 nm) was obtained by dipping the titanium discs
(Ti-discs) into a solution containing surfactants, water, organic solvent and
crystalline hydroxyapatite particles with a Ca/P ratio of 1.67. The diameter of the
hydroxyapatite particles was approximately 10 nm. After the dipping procedure, the
discs were let to dry in open air for 30 min, allowing the organic solvent to
evaporate. To remove all dispersing agents, the discs were subjected to heat
treatment at 550 °C for 5 min [<xref ref-type="bibr" rid="B28">28</xref>
].</p>
<p><bold>Laminin coating and quantification</bold>
</p>
<p>Laminin coating</p>
<p>Laminin (Sigma-Aldrich, L2020, Stockholm, Sweden) was diluted to a concentration of
100 µg/ml in PBS containing 0.15M NaCl, at pH 7.4 at room temperature. The titanium
discs belonging to groups B, AH, AO and HA were subsequently incubated for 1 h at
room temperature in 48 well plates (Nunclon Surface, Nunc, Roskilde, Denmark)
containing 250 µl per well of the laminin solution. The discs were then rinsed with
Milli-Q water and blown dry in order to avoid deposition of salts and remove
non-adsorbed proteins.</p>
<p>Optically smooth titanium surface preparation</p>
<p>For quantification of adsorbed laminin layer optically smooth titanium surfaces were
prepared as described by Linderbäck et al. [<xref ref-type="bibr" rid="B29">29</xref>
]. Cleaned SiO<sub>2</sub>
surfaces were placed in an evaporation
chamber with a final pressure below 1×10<sup>-8</sup>
Torr. Approximately 200 nm of
titanium was physical vapour deposited (PVD), and thereafter spontaneously oxidized
at room conditions. The static water contact angle of optically smooth titanium was
Θ < 10° at room conditions and > 50° after heating to 300 – 500°C at room
conditions for 30 min. The effect of UVO-treatment (Ultra Violet Ozone) was
investigated on a set of surfaces illuminated for up to 96 h in a UVO preparation
chamber (Jelight Company Inc., Irvine-USA). The wavelengths of the emitted light
were 253.7 nm (100%) and 184.9 nm (19%), respectively. The samples were placed within
2cm fromthe lamp (Novakemi AB, Handen-Sweden), and the UVO-chamber temperature was
below 100°C. Changes in surface hydrophilicity prior and subsequent to
UVO-illumination or annealing was characterized using an OCA 15 plus contact angle
microscope (CAM) used in sessile drop mode (Dataphysics Instruments GmBH,
Filderstadt, Germany).</p>
<p>Ellipsometry</p>
<p>The amount adsorbed laminin was calculated on the optically smooth titanium surfaces.
The surface treated discs were not possible to analyze, since these surfaces did not
reflect the laser beam in a measurable manner. Optically smooth titanium surfaces
were fixed in the ellipsometric quvette filled with PBS at room temperature. The
ellipsometry angles Δ<sub>0</sub>
and Ψ<sub>0</sub>
were measured with a Rudolph Research AutoEL
III ellipsometer operating in a wavelength of 632.8 nm at a 70° angle of incidence.
Thereafter, the quvette was emptied and filled with laminin solution and new angles
Δ and Ψ calculated. The protein layer thickness was iterated from the
ellipsometer angle changes under the assumption that the protein refractive index
was n = 1.465. The McCrackin algorithm was used for the calculations [<xref ref-type="bibr" rid="B30">30</xref>
].</p>
<p><bold>SBF immersion</bold>
</p>
<p>The revised SBF (r-SBF) used in this study was prepared according to the literature
[<xref ref-type="bibr" rid="B31">31</xref>
]. In brief, 5.403 g NaCl (Merck,
Darmstadt, Germany), 0.740 g NaHCO<sub>3</sub>
(Merck, Darmstadt, Germany), 2.046 g
Na<sub>2</sub>
CO<sub>3</sub>
(Merck, Darmstadt, Germany), 0.225 g KCl (Merck,
Darmstadt, Germany), 0.230 g K<sub>2</sub>
HPO<sub>4</sub>
· 3H<sub>2</sub>
O (Merck,
Darmstadt, Germany), 0.311 g MgCl<sub>2</sub>
· 6H<sub>2</sub>
O (Merck, Darmstadt, Germany),
11.928 g 2-(4-[2-hydroxyethyl]-1-piperazinyl) ethanesulfonic acid (HEPES) (Reach
Organics Inc., Cleveland, Ohio, USA), 0.293 g CaCl<sub>2</sub>
(KEBO Lab AB, Spånga, Sweden)
and 0.072 g Na<sub>2</sub>
SO<sub>4</sub>
(Merck, Darmstadt, Germany) were dissolved
in 1000 ml distilled water. HEPES was dissolved in 100 ml distilled water before
being added to the solution and the final pH was adjusted to 7.4 at 37 °C.</p>
<p>The discs were immersed in 25 ml r-SBF in separate sealed polystyrene vials at 37 °C.
After immersion for 1 h, 1 day, 3 days, 1 week and 2 weeks, the r-SBF immersion was
interrupted and the specimens rinsed with distilled water in order to remove any
loosely attached calcium phosphate. Thereafter, the specimens were left to dry at
room temperature and ultimately sealed in dry vials. Three samples of each type of
surface were not immersed in r-SBF (0 hours).</p>
<p><bold>Topographic characterization</bold>
</p>
<p>The specimens were topographically characterized after immersion in r-SBF with an
interferometer MicroXam (Phase-Shift, Tucson, Arizona, USA) operating in a wave
length of λ = 550 nm.</p>
<p>A Gaussian filter with size 50 × 50 µm<sup>2</sup>
was applied to separate roughness
from form and waviness. Thereafter, the surface roughness was calculated by using
the following topographical parameters defined as essential for describing the
topography of biomaterial surfaces [<xref ref-type="bibr" rid="B32">32</xref>
]:</p>
<p>S<sub>a</sub>
= Arithmetic mean height deviation from a mean plane (µm).</p>
<p>S<sub>ds</sub>
= Density of summits, i.e. the number of summits of a unit sampling
area (µm<sup>-2</sup>
).</p>
<p>S<sub>dr</sub>
= Developed interfacial area ratio, i.e. the ratio of the increment of
the interfacial area of a surface over the sampling area (%).</p>
<p>Calculations of group means and standard errors for each surface preparation and time
point were performed.</p>
<p><bold>Scanning electron microscopy/energy dispersive X-ray analysis
(SEM/EDX)</bold>
</p>
<p>For the SEM analysis, a LEO Ultra 55 FEG SEM equipped with an Oxford Inca EDX system,
operating at 8 and 10 kV was used. The samples were examined without surface
sputtering. Micrographs were recorded at different magnifications to investigate
both the surface coverage and the morphology of the crystals. EDX analysis at a
magnification of 150 times was performed to describe the atomic composition. Two
samples from each surface composition. Three titanium discs for each preparation and
incubation time were analyzed and a mean value calculated.</p>
<p><bold>Statistical analysis</bold>
</p>
<p>The normal distribution of the variables was confirmed by Kolmogorov - Smirnov test.
Statistical analysis was performed with Statistical Package for the Social Sciences
for Windows, version 18 (SPSS<sup>®</sup>
, Chicago, Illinois, USA) using one-way ANOVA
(Analysis of Variance). The multiple paired comparisons were performed by Bonferroni
Post-Hoc test. The statistical significance level was defined at 0.05.</p>
</sec>
<sec sec-type="results"><title>RESULTS</title>
<p><bold>Topographical analysis</bold>
</p>
<p>As demonstrated by Table 1, the laminin coating elicited no difference on the
examined topographic parameters S<sub>a</sub>
, S<sub>ds</sub>
and S<sub>dr</sub>
when comparing group B and group B- (P > 0.05). Treatment of the titanium discs
with alkali and heat resulted in the lowest S<sub>a</sub>
and the highest density of
summits (P < 0.05) among the tested surface modifications. As a total, the AH –
group possessed the highest developed interfacial area ratio resulting in larger
total surface</p>
<table-wrap id="T1" orientation="portrait" position="float"><label>Table 1</label>
<caption><p>S<sub>a</sub>
, S<sub>ds</sub>
and S<sub>dr</sub>
for the five different
surface groups. Mean values and standard errors are presented</p>
</caption>
<table frame="hsides" rules="groups" width="420"><thead><tr><td align="center" rowspan="1" colspan="1"><bold>Surface</bold>
</td>
<td align="center" rowspan="1" colspan="1"><bold>S<sub>a</sub>
(µm)</bold>
</td>
<td align="center" rowspan="1" colspan="1"><bold>S<sub>ds</sub>
(µm<sup>-2</sup>
)</bold>
</td>
<td align="center" rowspan="1" colspan="1"><bold>S<sub>dr</sub>
(%)</bold>
</td>
</tr>
</thead>
<tbody><tr><td align="center" rowspan="1" colspan="1"><bold>B-</bold>
</td>
<td align="center" rowspan="1" colspan="1"> 1.36 ± 0.05 </td>
<td align="center" rowspan="1" colspan="1"> 153873.2 ± 2585.8 </td>
<td align="center" rowspan="1" colspan="1"> 60.99 ± 2.33 </td>
</tr>
<tr><td align="center" rowspan="1" colspan="1"><bold>B</bold>
</td>
<td align="center" rowspan="1" colspan="1"> 1.30 ± 0.07 </td>
<td align="center" rowspan="1" colspan="1"> 157884.7 ± 6021.2 </td>
<td align="center" rowspan="1" colspan="1"> 60.13 ± 5.85 </td>
</tr>
<tr><td align="center" rowspan="1" colspan="1"><bold>AH</bold>
</td>
<td align="center" rowspan="1" colspan="1"> 1.24 ± 0.09<sup>a</sup>
</td>
<td align="center" rowspan="1" colspan="1"> 234634.8 ± 8454.7<sup>a</sup>
</td>
<td align="center" rowspan="1" colspan="1"> 84.61 ± 2.32<sup>a</sup>
</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1"><bold>AO</bold>
</td>
<td align="center" rowspan="1" colspan="1"> 1.38 ± 0.05 </td>
<td align="center" rowspan="1" colspan="1"> 171155.8 ± 5768.1 </td>
<td align="center" rowspan="1" colspan="1"> 73.84 ± 3.14 </td>
</tr>
<tr><td align="center" rowspan="1" colspan="1"><bold>HA</bold>
</td>
<td align="center" rowspan="1" colspan="1"> 1.33 ± 0.09 </td>
<td align="center" rowspan="1" colspan="1"> 168952.5 ± 3574.2 </td>
<td align="center" rowspan="1" colspan="1"> 66.00 ± 6.07 </td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p><sup>a</sup>
Significant at the level P < 0.05 (Bonferroni Post-Hoc
test).</p>
<p>B- = uncoated blasted titanium; B = blasted and laminin coated;</p>
<p>AH = alkali heat treated and laminin coated; AO = anodic oxidized and
laminin coated; HA = hydroxyapatite and laminin coated.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<p><bold>Ellipsometry</bold>
</p>
<p>The thickness of the adsorbed protein was estimated to 26 Å, approximating 180
ng/cm<sup>2</sup>
[<xref ref-type="bibr" rid="B30">30</xref>
]. The layer
approximates two monolayers in thickness.</p>
<p><bold>SEM/EDX</bold>
</p>
<p>SEM-images were acquired with a × 5000 magnification prior to and after 2 weeks of
incubation in r-SBF. The images prior to incubation demonstrated no differences in
surface morphology when comparing the uncoated (<xref ref-type="fig" rid="fig1">Figure 1a</xref>
) to the coated control blasted surface (<xref ref-type="fig" rid="fig1">Figure 1b</xref>
). On the contrary, the alkali and heat treated
titanium surfaces (<xref ref-type="fig" rid="fig1">Figure 1c</xref>
) demonstrated a
smooth surface, covered with microscopic spike-like structures and the anodic
oxidated ones possesed a porous appearance (<xref ref-type="fig" rid="fig1">Figure
1d</xref>
). However, no differences were detected in surface morphology when
comparing the nano-sized hydroxyapatite coated surface (<xref ref-type="fig" rid="fig1">Figure 1e</xref>
) to the controls (<xref ref-type="fig" rid="fig1">Figures 1a and 1b</xref>
). All three surfaces displayed a sharp-edged
appearance, which probably depended on the blasting procedure, and included some
Al<sub>2</sub>
O<sub>3</sub>
crystals. Nano-sized hydroxyapatite crystals could
not be observed at this magnification. In general, no laminin molecules were
observed at this magnification probably depending on the fact that the magnification
was not high enough to reveal nano-sized features.</p>
<fig id="fig1" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>SEM images of titanium disks prior to incubation in SBF (× 5000): (a) B- =
uncoated blasted; (b) B = blasted and laminin coated; (c) AH = alkali heat
treated and laminin coated; (d) AO = anodic oxidized and laminin coated; (e)
HA = hydroxyapatite and laminin coated.</p>
</caption>
<graphic xlink:href="jomr-02-e5-g001"></graphic>
</fig>
<p>The bar presents 10µm.</p>
<p>After 2 weeks of incubation in SBF, the surfaces B, AH and AO were fully covered with
a homogenous calcium phosphate layer (<xref ref-type="fig" rid="fig2">Figures 2b, 2c
and 2d</xref>
). On the contrary, the HA surface (<xref ref-type="fig" rid="fig2">Figure 2e</xref>
) and the B- surface (<xref ref-type="fig" rid="fig2">Figure
2a</xref>
) appeared to be only partially covered by crystals.</p>
<fig id="fig2" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>SEM image of a titanium disks after incubation in SBF for 2 weeks (× 5000):
(a) B- = uncoated blasted; (b) B = blasted and laminin coated; (c) AH =
alkali heat treated and laminin coated; (d) AO = anodic oxidized and laminin
coated; (e) HA = hydroxyapatite and laminin coated. The bar presents 10
µm.</p>
</caption>
<graphic xlink:href="jomr-02-e5-g002"></graphic>
</fig>
<p><bold>EDX</bold>
</p>
<p>Calcium phosphate (CaP)</p>
<p> The total amount of calcium phosphate on surfaces of titanium discs was assessed
with EDX by measuring and adding the relative elemental amount of calcium (Ca) and
phosphorous (P) present on the surface. AH surfaces showed the highest Ca and P
content after 72 h, 1 week and 2 weeks. After 2 weeks no significant differences
were detected among the test surfaces AO, HA and the positive control B. At the same
time, the negative control B- demonstrated the lowest Ca and P precipitation (<xref ref-type="fig" rid="fig3">Figure 3</xref>
).</p>
<fig id="fig3" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>Total amount of precipitated calcium and phosphate on titanium disks
calculated by EDX: B- = uncoated blasted; B = blasted and laminin coated; AH
= alkali heat treated and laminin coated; AO = anodic oxidized and laminin
coated; HA = hydroxyapatite and laminin coated. Mean values and standard
errors are presented.</p>
</caption>
<graphic xlink:href="jomr-02-e5-g003"></graphic>
</fig>
<p>Calcium/Phosphorous ratio (Ca/P ratio)</p>
<p>The proposed bioactive surfaces, i.e. AH, AO and HA treated samples, demonstrated a
higher Ca/P ratio than both blasted control samples (B and B-) during the first 24
hours. Noteworthy, calcium and phosphate signals were detected at an earlier time
point on bioactive surfaces compared to blasted surfaces, depending on the bioactive
modification process. The high early Ca content on the AH surface contributed to a
high Ca/P ratio. After 2 weeks of SBF immersion, all the surface groups presented a
Ca/P ratio around 1.67, corresponding to hydroxyapatite crystalline formation (<xref ref-type="fig" rid="fig4">Figure 4</xref>
). Interestingly, the high Ca/P ratio
of AH and AO surfaces at early time points decreases with increasing SBF incubation
time.</p>
<fig id="fig4" orientation="portrait" position="float"><label>Figure 4</label>
<caption><p>Calcium/phosphorous ratio on titanium disks calculated by EDX: B- = uncoated
blasted titanium; B = blasted and laminin coated; AH = alkali heat treated
and laminin coated; AO = anodic oxidized and laminin coated; HA =
hydroxyapatite and laminin coated. Mean values and standard errors are
presented.</p>
</caption>
<graphic xlink:href="jomr-02-e5-g004"></graphic>
</fig>
</sec>
<sec sec-type="discussion"><title>DISCUSSION</title>
<p>Protein coatings have previously been used as a method to stimulate bone formation
around implants in different experimental models with promising results [<xref ref-type="bibr" rid="B33">33</xref>
-<xref ref-type="bibr" rid="B36">36</xref>
].
Although there is a general agreement that a proper protein coating is promising in
terms of enhanced osseointegration, there is still little known regarding the
involved mechanisms. The main objective of this study was to study the etiology of
the phenomenon in a controlled <italic>in vitro</italic>
milieu as the SBF model.</p>
<p>The results demonstrate that all laminin coated surfaces induced a higher final CaP
deposition as compared to uncoated blasted titanium after 2 weeks. The fact that all
the "bioactively" modified surfaces, i.e. AH, AO, HA, demonstrate a higher
CaP formation is in agreement with the findings of Arvidsson et al. [<xref ref-type="bibr" rid="B37">37</xref>
]. The present study demonstrates that a thin
laminin coating on a blasted titanium surface results to enhanced CaP precipitation
as compared to a surface without laminin (B-) and to similar CaP precipitation as
compared to bioactively modified surfaces. Therefore, we have reasons to believe
that a laminin coating may be utilized as a method to bioactively modify a non
bioactive surface.</p>
<p>The SEM image demonstrating a laminin coated blasted disc after 2 weeks in SBF (<xref ref-type="fig" rid="fig2">Figure 2b</xref>
), is similar to the images
corresponding the AH (<xref ref-type="fig" rid="fig2">Figure 2c</xref>
) and AO
specimens (<xref ref-type="fig" rid="fig2">Figure 2d</xref>
). In those images, the
underlying titanium is not visible depended on deposition of CaP and large crystals.
Interestingly, as examined with EDX, after 2 weeks the Ca/P ratio is approximately
1.67 corresponding to hydroxyapatite, indicating that the formed CaP is
hydroxyapatite. A possible explanation for the high performance of the AH surface,
in terms of CaP precipitation, may be the fact that the developed interfacial area
ratio S<sub>dr</sub>
according to <xref ref-type="table" rid="T1">Table 1</xref>
is
the highest among the tested surfaces, thereby providing a larger interface area
with the SBF. This observation demonstrates that it is imperative to take into
account at least one hybrid factor when characterizing surface topography, since
considering solely S<sub>a</sub>
may lead to false conclusions.</p>
<p>The results of a previous study from our group [<xref ref-type="bibr" rid="B38">38</xref>
] suggest that a possible mechanism for laminin promoting CaP
precipitation <italic>in vitro</italic>
, may be its function as a nucleation centre. According to a
morphological study examining the same laminin molecule that we utilized in the
present study, laminin tends to assume a globular form when used for surface coating
[<xref ref-type="bibr" rid="B39">39</xref>
]. Some of the domains exposed on this
protein conformation may act as nucleation centres for calcium ions thereby
increasing the local calcium concentration, leading to enhanced nucleation ratio. In
a recent study on osteoblasts the effect of elevated extracellular calcium
concentration was proposed to stimulate osteoblasts through the receptor activator
of NF-κB ligand [<xref ref-type="bibr" rid="B40">40</xref>
]. Hence, it may be
possible that the enhanced calcium and phosphate precipitation triggers osteoblast
differentiation around a laminin coated implant also when applied <italic>in vivo</italic>
. There is
some indication that enhanced CaP precipitation may be relatively specific for
laminin since coating with bovine serum albumin instead reduced CaP precipitation
when compared to non-coated hydroxyapatite surfaces [<xref ref-type="bibr" rid="B41">41</xref>
]. An additional mechanism suggesting that laminin may be a bone
stimulating coating agent is the possible interaction of the
arginine-glycine-aspartic acid (RGD) motif with the integrin receptors of the
surrounding cells. It has been reported that when RGD-sequences are coated on
implants, osseointegration [<xref ref-type="bibr" rid="B36">36</xref>
,<xref ref-type="bibr" rid="B42">42</xref>
] seems to be enhanced, and the osteoblast
adhesion appears to be upregulated through integrin-mediated mechanisms [<xref ref-type="bibr" rid="B43">43</xref>
]. Nevertheless, the complexity of the <italic>in
vivo</italic>
environment makes it imperative to further investigate parameters such as the
retention and the clearance of the coating before any further conclusions may be
drawn regarding the suitability of laminin as a biomaterial coating agent.</p>
</sec>
<sec sec-type="conclusions"><title>CONCLUSIONS</title>
<p>The results of the present study demonstrate that after 2 weeks of incubation in SBF
all the laminin coated titanium surfaces, including the laminin coated blasted
controls, induced a higher CaP deposition as compared to uncoated blasted titanium
discs. Among the tested surface modifications, alkali and heat treatment seemed to
induce a more rapid CaP precipitation. Our study demonstrates that laminin may have
the potential to be used as a coating agent in order to enhance the osseoinductive
performance of biomaterial surfaces with the protein molecules possibly functioning
as nucleation centres for apatite formation. <italic>In vivo</italic>
studies are however needed in
order to further investigate the possible effect of laminin as a coating agent in
the osseointegration of titanium implants.</p>
</sec>
</body>
<back><ack><sec sec-type="acknowledgments and disclosure statements"><title>ACKNOWLEDGMENTS AND DISCLOSURE STATEMENTS</title>
<p>The authors thank Agneta Askendal from the department of Applied Physics in
Linköping University, Sweden for her assistance on the protein coating process.
This study was supported by the Swedish National Graduate School in
Odontological Science. The authors also acknowledge the Swedish Research Council
(K2009-52X-06533-27-3), Hjalmar Svenson Research Foundation, Sylvan Foundation,
Wilhelm and Martina Lundgren Science Foundation, the Royal Society of Arts and
Sciences in Göteborg and the Council for Research and Development in Södra
Älvsborg, Sweden for funding the project.</p>
</sec>
</ack>
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