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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en"><italic>In vitro</italic> Evaluation of Calcium Phosphate Precipitation on Possibly Bioactive Titanium Surfaces in the Presence of Laminin</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></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24421995</idno><idno type="pmc">3886075</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3886075</idno><idno type="RBID">PMC:3886075</idno><idno type="doi">10.5037/jomr.2011.2303</idno><date when="2011">2011</date><idno type="wicri:Area/Pmc/Corpus">000692</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000692</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main"><italic>In vitro</italic> Evaluation of Calcium Phosphate Precipitation on Possibly Bioactive Titanium Surfaces in the Presence of Laminin</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></author></analytic><series><title level="j">Journal of Oral & Maxillofacial Research</title><idno type="eISSN">2029-283X</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>ABSTRACT</title><sec sec-type="objectives"><title>Objectives</title><p>The aim of the present study was to evaluate calcium phosphate precipitation
and the amount of precipitated protein on three potentially bioactive
surfaces when adding laminin in simulated body fluid.</p></sec><sec sec-type="material and methods"><title>Material and Methods</title><p>Blasted titanium discs were prepared by three different techniques claimed to
provide bioactivity: alkali and heat treatment (AH), anodic oxidation (AO)
or hydroxyapatite coating (HA). A blasted surface incubated in
laminin-containing simulated body fuid served as a positive control (B)
while a blasted surface incubated in non laminin-containing simulated body
fuid served as a negative control (B-). The immersion time was 1 hour, 24
hours, 72 hours and 1 week. Surface topography was investigated by
interferometry and morphology by Scanning Electron Microscopy (SEM).
Analysis of the precipitated calcium and phosphorous was performed by Energy
Dispersive X-ray Spectroscopy (EDX) and the adsorbed laminin was quantified
by iodine (<sup>125</sup>I) labeling.</p></sec><sec sec-type="results"><title>Results</title><p>SEM demonstrated that all specimens except for the negative control were
totally covered with calcium phosphate (CaP) after 1 week. EDX revealed that
B- demonstrated lower sum of Ca and P levels compared to the other groups
after 1 week. Iodine labeling demonstrated that laminin precipitated in a
similar manner on the possibly bioactive surfaces as on the positive control
surface.</p></sec><sec sec-type="conclusions"><title>Conclusions</title><p>Our results indicate that laminin precipitates equally on all tested titanium
surfaces and may function as a nucleation center thus locally elevating the
calcium concentration. Nevertheless further studies are required to clarify
the role of laminin in the interaction of biomaterials with the host bone
tissue.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Hench, L" uniqKey="Hench L">L Hench</name></author><author><name sortKey="Yamamuro, T" uniqKey="Yamamuro T">T Yamamuro</name></author><author><name sortKey="Wilson, J" uniqKey="Wilson J">J Wilson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Williams, Df" uniqKey="Williams D">DF Williams</name></author><author><name sortKey="Editor" uniqKey="Editor">editor</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ellingsen, Je" uniqKey="Ellingsen J">JE Ellingsen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kim, Hm" uniqKey="Kim H">HM Kim</name></author><author><name sortKey="Miyaji, F" uniqKey="Miyaji F">F Miyaji</name></author><author><name sortKey="Kokubo, T" uniqKey="Kokubo T">T Kokubo</name></author><author><name sortKey="Nakamura, T" uniqKey="Nakamura T">T 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<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">24421995</article-id><article-id pub-id-type="pmc">3886075</article-id><article-id pub-id-type="publisher-id">v2n3e3ht</article-id><article-id pub-id-type="doi">10.5037/jomr.2011.2303</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Paper</subject></subj-group></article-categories><title-group><article-title><italic>In vitro</italic> Evaluation of Calcium Phosphate Precipitation on Possibly Bioactive Titanium Surfaces in the Presence of Laminin</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>Jul-Sep</season><year>2011</year></pub-date><pub-date pub-type="epub"><day>1</day><month>10</month><year>2011</year></pub-date><volume>2</volume><issue>3</issue><elocation-id>e3</elocation-id><history><date date-type="received"><day>2</day><month>7</month><year>2011</year></date><date date-type="accepted"><day>19</day><month>7</month><year>2011</year></date></history><permissions><copyright-statement> Copyright © Bougas K, Stenport VF, Currie F, Wennerberg
A. Published in the JOURNAL OF ORAL & MAXILLOFACIAL RESEARCH
(http://www.ejomr.org), 1 October 2011.</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/2011/3/e3/v2n3e3ht.htm"></self-uri><abstract><title>ABSTRACT</title><sec sec-type="objectives"><title>Objectives</title><p>The aim of the present study was to evaluate calcium phosphate precipitation
and the amount of precipitated protein on three potentially bioactive
surfaces when adding laminin in simulated body fluid.</p></sec><sec sec-type="material and methods"><title>Material and Methods</title><p>Blasted titanium discs were prepared by three different techniques claimed to
provide bioactivity: alkali and heat treatment (AH), anodic oxidation (AO)
or hydroxyapatite coating (HA). A blasted surface incubated in
laminin-containing simulated body fuid served as a positive control (B)
while a blasted surface incubated in non laminin-containing simulated body
fuid served as a negative control (B-). The immersion time was 1 hour, 24
hours, 72 hours and 1 week. Surface topography was investigated by
interferometry and morphology by Scanning Electron Microscopy (SEM).
Analysis of the precipitated calcium and phosphorous was performed by Energy
Dispersive X-ray Spectroscopy (EDX) and the adsorbed laminin was quantified
by iodine (<sup>125</sup>I) labeling.</p></sec><sec sec-type="results"><title>Results</title><p>SEM demonstrated that all specimens except for the negative control were
totally covered with calcium phosphate (CaP) after 1 week. EDX revealed that
B- demonstrated lower sum of Ca and P levels compared to the other groups
after 1 week. Iodine labeling demonstrated that laminin precipitated in a
similar manner on the possibly bioactive surfaces as on the positive control
surface.</p></sec><sec sec-type="conclusions"><title>Conclusions</title><p>Our results indicate that laminin precipitates equally on all tested titanium
surfaces and may function as a nucleation center thus locally elevating the
calcium concentration. Nevertheless further studies are required to clarify
the role of laminin in the interaction of biomaterials with the host bone
tissue.</p></sec></abstract><kwd-group><kwd>laminin</kwd><kwd>titanium</kwd><kwd>body fluid</kwd><kwd>calcium phosphates</kwd><kwd>biomaterials.</kwd></kwd-group></article-meta></front><body><sec><title>INTRODUCTION</title><p>Bone anchored titanium implants are used in the rehabilitation of edentulism. The
bone formation around titanium implants has been extensively investigated, however
despite this the biological phenomenon is yet to be understood to the full extend.
It has been suggested that a biochemical bonding between bone tissue and titanium
surfaces can be obtained by using bioactive implants. Bioactivity has been defined
as "the characteristics of an implant material which allows it to form a bond with
living tissues" [<xref ref-type="bibr" rid="B1">1</xref>]. However, bioactivity is
today defined in more general terms implying a chemical influence on bone tissue
[<xref ref-type="bibr" rid="B2">2</xref>]. Theoretically, the advantages with
bioactive implants could be rapid biochemical stimulation, and that the interaction
between implant and bone may enhance early bone formation.</p><p>Chemical modification methods of titanium implant surfaces have been proposed to
enhance bone growth. Some of these techniques are fluoride etching [<xref ref-type="bibr" rid="B3">3</xref>], alkali-heat treatment [<xref ref-type="bibr" rid="B4">4</xref>], anodic oxidation [<xref ref-type="bibr" rid="B5">5</xref>,<xref ref-type="bibr" rid="B6">6</xref>], coatings of calcium
phosphates in sol-gels [<xref ref-type="bibr" rid="B7">7</xref>], and immobilization
of organic bio-molecules or polymers on the surface [<xref ref-type="bibr" rid="B8">8</xref>,<xref ref-type="bibr" rid="B9">9</xref>]. These techniques alter not
only the surface chemistry but also the topography, which both may contribute to an
increased attachment to the bone. However, the exact mechanism of bone formation on
the different surfaces has not been fully clarified.</p><p>A variety of materials and surface modifications have been evaluated <italic>in vitro</italic> by
using the simulated body fluid (SBF) model [<xref ref-type="bibr" rid="B10">10</xref>-<xref ref-type="bibr" rid="B12">12</xref>]. SBF is defined as an
acellular, protein-free solution with ion concentrations approximately equal to
those of human blood plasma [<xref ref-type="bibr" rid="B13">13</xref>,<xref ref-type="bibr" rid="B15">15</xref>]. The nucleating capacity of a biomaterial
can be observed by immersing it in SBF [<xref ref-type="bibr" rid="B16">16</xref>].
It has been suggested that the nucleation of calcium/phosphates mimics the initial
mineralization of bone on the implant surface. In a review on the usefulness of SBF
in predicting the <italic>in vivo</italic> bone bioactivity, a correlation has been
described between apatite formation in SBF models and bone bioactivity <italic>in
vivo</italic> [<xref ref-type="bibr" rid="B17">17</xref>].</p><p>However, compared to the SBF model, the <italic>in vivo</italic> process is much more
complex and numerous proteins, enzymes and biological factors play an important role
in this process [<xref ref-type="bibr" rid="B18">18</xref>]. Some studies applied
bovine serum albumine (BSA) in various concentrations in SBF-solutions. The results
indicated that the BSA alters the nucleation rate, morphology, composition and
crystallinity of the Ca/P precipitates [<xref ref-type="bibr" rid="B18">18</xref>-<xref ref-type="bibr" rid="B20">20</xref>]. This is of interest,
since it has been discussed if protein adsorption may contribute to cell behaviour,
and thus can be regarded as a fundamental reaction [<xref ref-type="bibr" rid="B21">21</xref>]. Thereby, it has been speculated that the protein adsorption could
play a role in the bioactivity of specific materials.</p><p>Laminins are heterotrimeric glycoprotein molecules included in the proteins that are
involved in cell adhesion on biomaterials [<xref ref-type="bibr" rid="B22">22</xref>] possessing the ability to bind to a protein family known as integrins,
especially β1 and β2 integrins [<xref ref-type="bibr" rid="B23">23</xref>]. Integrins are integral membrane glycoproteins which mediate
cell-to-cell and cell-to-matrix interactions. Integrins have not only the ability to
mediate cell adhesion to extracellular matrix, but they also facilitate the cell
communication [<xref ref-type="bibr" rid="B24">24</xref>]. By their cytoplasmic
domains, they participate in the assembly of the cytoskeleton and thereby
influencing cell migration, adhesion of epithelial cells and hemidesmosome formation
[<xref ref-type="bibr" rid="B23">23</xref>]. <italic>In vitro</italic> studies suggest that
laminin-1 recruits osteoprogenitors cells through an attachment effect [<xref ref-type="bibr" rid="B25">25</xref>,<xref ref-type="bibr" rid="B26">26</xref>],
and to human osteoblast-like cells through the β1 integrin subunit [<xref ref-type="bibr" rid="B27">27</xref>].</p><p>The aim with the present study was to evaluate the nucleating behaviour of three
different surfaces, claimed to be bioactive and to compare them with a blasted
control surface in the presence of laminin in a simulated body fuid model since
laminin seems to act as a promising osteoprogenitor recruiting protein.</p></sec><sec sec-type="materials|methods"><title>MATERIAL AND METHODS</title><p><bold>Surface preparations</bold></p><p>In total, 75 discs (diameter = 8 mm, thickness = 1 mm) of titanium grade 4 were used
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 were
subsequently cleaned ultrasonically in diluted Extran MA01 and absolute ethanol, and
were dried at 60 °C for 24 h. The specimens were then divided into five equally
sized groups (n = 15). A group of blasted discs incubated in laminin-containing SBF
served as a positive control (B), while a group of blasted specimens incubated in
non laminin-containing SBF served as a negative control (B-). The other three groups
were treated as following.</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="B15">15</xref>,<xref ref-type="bibr" rid="B28">28</xref>,<xref ref-type="bibr" rid="B29">29</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. 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 using the
Micro Arc Oxidation (MAO) method in galvanostatic mode as described by Sul et al.
[<xref ref-type="bibr" rid="B30">30</xref>]. More specifically, the
electrochemical cell was composed of platinum plates as cathodes, and 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="B31">31</xref>]. Surface
analysis of the oxidizedgroup demonstrated the following properties: a calcium
content of 11 atomic percent in the newly formed oxide with a 1.2 µm thickness, 24 %
porosity of porous structure and anatase and rutile crystal structure [<xref ref-type="bibr" rid="B32">32</xref>,<xref ref-type="bibr" rid="B33">33</xref>].</p><p>Hydroxyapatite coating (HA)</p><p>A thin hydroxyapatite layer (< 50 nm) was obtained by dipping the titanium discs
into a solution containing surfactants, water, organic solvent and crystalline
nanoparticles of hydroxyapatite 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="B34">34</xref>].</p><p><bold>Radio Labelling of Laminin</bold></p><p>Laminin (Sigma-Aldrich, Stockholm, Sweden) was labelled with iodine-125 (<sup>125</sup>I)
(Amersham Pharmacia Biotech, Uppsala, Sweden) using the Iodo-Bead iodination method
(Pierce, USA). The beads were rinsed in phosphate buffered saline (PBS) at pH 6.5
with 0.25 mM sodium azide. The sodium iodide-125 was mixed in PBS, and equilibrated
for 5 min. Subsequently, laminin in PBS was added, and incubated for 7 min under
gentle stirring. The solution with the labeled protein was dialyzed with 50 mM KI
added against PBS using dialysis tubings (Spectrapor, Rancho Dominguez, CA, USA)
with a pore size of 3500 Da. Small volumes were taken at different times from the
dialysate, and the activity was checked throughout the procedure. The labelled
protein solution was dialyzed in several steps until the activity fell below 5000
CPM/ml. The protein concentration was determined by spectrophotometry (Shimadzu
UV-1601PC, Columbia, MD, USA) at 280 nm. A series of solutions with known
concentrations of respective unlabeled protein was used for the calibration.</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="B35">35</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 MgCl2·6H<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 1,000 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. Laminin marked with <sup>125</sup>I was added to adjust to a final concentration of 300 ng/ml, which corresponds to the
concentration of laminin included in the human blood plasma [<xref ref-type="bibr" rid="B36">36</xref>].</p><p>The discs were immersed in 25 ml r-SBF/laminin in separate sealed polystyrene vials,
and incubated at 37 °C. After immersion for 1 h, 1 day, 3 days and 1 week the
r-SBF/laminin immersion was interrupted, and the specimens were rinsed with
distilled water, in order to remove any loosely attached calcium phosphates.
Thereafter, the specimens were left to dry at room temperature, and ultimately
sealed in dry vials. Three samples for each type of surface were not immersed in
r-SBF/laminin (0 h).</p><p><bold>Laminin quantification</bold></p><p>After immersion in r-SBF/laminin, the specimens were transferred to a gamma counter
(Packard Cobra II, Canberra, USA), and the activity was measured for 10 min. To
correlate the gamma counter values to the adsorbed amounts, known volumes with known
labelled protein concentrations were measured in the gamma counter. The surfaces and
proteins did not adsorb free <sup>125</sup>I from the solutions, and the proteins were not
noticeably affected by the labelling procedure [<xref ref-type="bibr" rid="B37">37</xref>].</p><p><bold>Topographic characterization</bold></p><p>The specimens were topographically analyzed after immersion in r-SBF/laminin 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 using the following
topographical parameters defined as essential for describing the topography of
biomaterial surfaces [<xref ref-type="bibr" rid="B38">38</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 deviations 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
discs for each preparation and incubation time were analyzed, and mean value was
calculated.</p><p><bold>Statistical analysis</bold></p><p>The normal distribution of the variables was controlled by Kolmogorov-Smirnov
normality 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 statistical significance level was set at
0.05. Multiple paired comparisons were performed by Bonferroni Post-Hoc test with
the statistical significance level defined at 0.05.</p></sec><sec sec-type="results"><title>RESULTS</title><p><bold>Topographical characterization</bold></p><p>The AH surface demonstrated small height deviation and large density of
irregularities. The surface enlargement is explained by the large S<sub>ds</sub>value. After 1 week of incubation, no differences with respect to surface roughness
was possible to detect among the surface groups incubated in laminin-containing SBF.
Regarding the negative control B-, S<sub>ds</sub> and S<sub>dr</sub> remained stable
throughout the incubation, and were significantly lower when compared to the
specimens incubated in presence of laminin.</p><p>S<sub>a</sub> mean values</p><p>The AH surface and the negative control had a lower mean S<sub>a</sub> than the other
surfaces prior to immersion. The AH surface and the negative control B- still had
the lowest S<sub>a</sub> of all surface groups after 72 h while no significant
differences in mean S<sub>a</sub> could be detected among the surface groups after 1
week of incubation (<xref ref-type="fig" rid="fig1">Figure 1</xref>).</p><fig id="fig1" orientation="portrait" position="float"><label>Figure 1</label><caption><p>Mean values and standard errors of S<sub>a</sub> for the four different
surface groups. B = blasted titanium; AH = alkali and heat treated; AO =
anodically oxidized; HA = hydroxyapatite coated; B- = blasted titanium
incubated in non laminin containing SBF. Mean values and standard errors are
presented.</p></caption><graphic xlink:href="jomr-02-e3-g001"></graphic></fig><p>S<sub>ds</sub> mean values</p><p>The AH surface had at all time points, the highest surface density of all the surface
groups except for the AH surface after 72 h of incubation. Group B had throughout
the incubation period the lowest density of summits. After having incubated the
samples for 1 week, the negative control B- still demonstrated the lowest
S<sub>ds</sub> value (<xref ref-type="fig" rid="fig2">Figure 2</xref>).</p><fig id="fig2" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Mean values and standard errors of S<sub>ds</sub> for the four different
surface groups. B = blasted titanium; AH = alkali and heat treated; AO =
anodically oxidized; HA = hydroxyapatite coated; B- = blasted titanium
incubated in non laminin containing SBF. Mean values and standard errors are
presented.</p></caption><graphic xlink:href="jomr-02-e3-g002"></graphic></fig><p>S<sub>dr</sub> mean values</p><p>The blasted surface (B) had the highest S<sub>dr</sub> mean value of all the other
surface groups prior to immersion in SBF and the negative control the lowest (B-).
After 1 week, no significant differences could be detected among the groups except
for the negative control B- being the only surface with significantly lower
S<sub>dr</sub> throughout the incubation period (<xref ref-type="fig" rid="fig3">Figure 3</xref>).</p><fig id="fig3" orientation="portrait" position="float"><label>Figure 3</label><caption><p>S<sub>dr</sub> of the four different surface groups. B = blasted titanium; AH
= alkali and heat treated; AO = anodically oxidized; HA = hydroxyapatite
coated; B- = blasted titanium incubated in non laminin containing SBF. Mean
values and standard errors are presented.</p></caption><graphic xlink:href="jomr-02-e3-g003"></graphic></fig><p><bold>SEM/EDX</bold></p><p>SEM images with a × 5,000 magnification acquired prior to incubation in SBF,
demonstrated differences in surface morphology when comparing the control blasted
surface (<xref ref-type="fig" rid="fig4">Figures 4 a and 4 e</xref>) to the alkali
and heat treated, which possessed a smooth surface, covered with microscopic
spike-like structures (<xref ref-type="fig" rid="fig4">Figure 4b</xref>) and to
anodic oxidated ones which had a porous appearance (<xref ref-type="fig" rid="fig4">Figure 4c</xref>). However, no differences were observed in surface morphology
when comparing the nano-sized hydroxyapatite coated surface (<xref ref-type="fig" rid="fig4">Figure 4d</xref>) to the control surface B. Both surfaces had
sharp-edged appearances, 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 in this magnification. After 1 week, no differences in surface morphology
could be observed when comparing the SEM images, since all the samples were totally
covered with a homogenous layer of crystals (<xref ref-type="fig" rid="fig5">Figures
5 a - d</xref>). Nevertheless, the blasted surface incubated solely in SBF
appeared to be only partially covered by crystals (<xref ref-type="fig" rid="fig5">Figure 5 e</xref>).</p><fig id="fig4" orientation="portrait" position="float"><label>Figure 4</label><caption><p>SEM images of Ti-discs prior to incubation in SBF (x 5,000) (a) B = blasted;
(b) AH = alkali and heat treated; (c) AO = anodically oxidized; (d) HA =
hydroxyapatite coated; (e) B- = blasted titanium incubated in non laminin
containing SBF. The bar presents 10 µm.</p></caption><graphic xlink:href="jomr-02-e3-g004"></graphic></fig><fig id="fig5" orientation="portrait" position="float"><label>Figure 5</label><caption><p>SEM image of a Ti-discs after incubation in SBF for 1 week (x 5,000) (a) B =
blasted; (b) AH = alkali and heat treated; (c) AO = anodically oxidized; (d)
HA = hydroxyapatite coated; (e) B- = blasted titanium incubated in non
laminin containing SBF. The size of the bar is 10 µm.</p></caption><graphic xlink:href="jomr-02-e3-g005"></graphic></fig><p><bold>EDX</bold></p><p>Calcium phosphate (CaP)</p><p>The total amount of calcium phosphate (CaP) crystals on the surface of the titanium
discs was measured with EDX by measuring and adding the relative elemental amount of
calcium (Ca) and phosphorous (P) present on the surface. The mean sum of Ca and P
was statistically significant higher (p < 0.05) for the AH surface throughout the
incubation time with a greater difference at 24 h and 72 h, and the differences were
statistically significant (p < 0.05). After 1 week no significant differences
could be detected among the groups incubated in laminin containing SBF. The negative
control B- failed to follow the same CaP precipitation pattern as the surfaces
incubated in laminin containing SBF and after 24 h it demonstrated lower levels of
total CaP, despite showing an ascending trend (<xref ref-type="fig" rid="fig6">Figure 6</xref>).</p><fig id="fig6" orientation="portrait" position="float"><label>Figure 6</label><caption><p>Total amount of precipitated calcium and phosphorous calculated from EDX
measurements. B = blasted titanium; AH = alkali and heat treated; AO =
anodically oxidized; HA = hydroxyapatite coated; B- = blasted titanium
incubated in non laminin containing SBF. Mean values and standard errors are
presented.</p></caption><graphic xlink:href="jomr-02-e3-g006"></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 the blasted control samples prior to incubation in SBF.
Furthermore, calcium and phosphorous signals were recorded at an earlier stage on
the bioactive surfaces compared to the blasted group. At the non-incubated samples,
no phosphorous (P) was detected on the AH surface, which in <xref ref-type="fig" rid="fig7">Figure 7</xref> is reported as missing value. The high initial Ca
content on the surface, contributed to a high Ca/P ratio where after 1 h of
incubation we could also detect P. After 1 h, all the possibly bioactive surfaces
had still higher Ca/P ratio than the blasted groups with the AH treated group
showing the highest ratio, and after 24 h the blasted group incubated in laminin
containing SBF had a significantly higher Ca/P ratio than the negative control B-.
After 72 h, all the groups had a Ca/P ratio around 1.67, corresponding to
hydroxyapatite crystalline formation. When the Ca/P ratio was examined after 1 week
of incubation, no statistically significant differences were detected among the
different surface groups (<xref ref-type="fig" rid="fig7">Figure 7</xref>).</p><fig id="fig7" orientation="portrait" position="float"><label>Figure 7</label><caption><p>Calcium/phosphate ratio calculated from EDX measurements. B = blasted
titanium; AH = alkali and heat treated; AO = anodically oxidized; HA =
hydroxyapatite coated; B- = blasted titanium incubated in non laminin
containing SBF. Mean values and standard errors are presented.</p></caption><graphic xlink:href="jomr-02-e3-g007"></graphic></fig><p><bold>Amount precipitated laminin</bold></p><p>The mean values for the amount precipitated laminin from the SBF on different
surfaces and time points are presented in <xref ref-type="table" rid="T1">Table 1</xref>. The groups B, AH and AO reached
their maximum laminin precipitation levels already after 1 h while the HA group
reached its top level after 24 h of incubation. However, no significant differences
of laminin levels could be detected among the different surface groups after equally
long incubation time.</p><table-wrap id="T1" orientation="portrait" position="float"><label>Table 1</label><caption><p>Adsorbed laminin on the four different surface groups. The table presents
mean values. Standard deviations are presented within parenthesis</p></caption><table frame="hsides" rules="groups" width="385"><thead><tr><td align="center" rowspan="1" colspan="1"><bold>SBF immersion time</bold></td><td align="center" rowspan="1" colspan="1"><bold>Surface type</bold></td><td align="center" rowspan="1" colspan="1"><bold>Laminin (ng) (SD)</bold></td></tr></thead><tbody><tr><td rowspan="4" align="center" colspan="1"><bold>0 hours</bold></td><td align="center" rowspan="1" colspan="1"> B </td><td align="center" rowspan="1" colspan="1"> 94.00 (1.16) </td></tr><tr><td align="center" rowspan="1" colspan="1"> AH </td><td align="center" rowspan="1" colspan="1"> 94.33 (1.86) </td></tr><tr><td align="center" rowspan="1" colspan="1"> AO </td><td align="center" rowspan="1" colspan="1"> 100.00 (1.16) </td></tr><tr><td align="center" rowspan="1" colspan="1"> HA </td><td align="center" rowspan="1" colspan="1"> 95.33 (2.40) </td></tr><tr><td colspan="3" rowspan="1"><hr></hr></td></tr><tr><td rowspan="4" align="center" colspan="1"><bold>1 hour</bold></td><td align="center" rowspan="1" colspan="1"> B </td><td align="center" rowspan="1" colspan="1"> 767.33 (107.16) </td></tr><tr><td align="center" rowspan="1" colspan="1"> AH </td><td align="center" rowspan="1" colspan="1"> 805.67 (129.97) </td></tr><tr><td align="center" rowspan="1" colspan="1"> AO </td><td align="center" rowspan="1" colspan="1"> 828.67 (176.62) </td></tr><tr><td align="center" rowspan="1" colspan="1"> HA </td><td align="center" rowspan="1" colspan="1"> 953.67 (24.10) </td></tr><tr><td colspan="3" rowspan="1"><hr></hr></td></tr><tr><td rowspan="4" align="center" colspan="1"><bold>24 hours</bold></td><td align="center" rowspan="1" colspan="1"> B </td><td align="center" rowspan="1" colspan="1"> 619.33 (95.59) </td></tr><tr><td align="center" rowspan="1" colspan="1"> AH </td><td align="center" rowspan="1" colspan="1"> 769.33 (120.76) </td></tr><tr><td align="center" rowspan="1" colspan="1"> AO </td><td align="center" rowspan="1" colspan="1"> 859.33 (246.07) </td></tr><tr><td align="center" rowspan="1" colspan="1"> HA </td><td align="center" rowspan="1" colspan="1"> 1111.33 (415.43) </td></tr><tr><td colspan="3" rowspan="1"><hr></hr></td></tr><tr><td rowspan="4" align="center" colspan="1"><bold>3 days</bold></td><td align="center" rowspan="1" colspan="1"> B </td><td align="center" rowspan="1" colspan="1"> 501.67 (69.96) </td></tr><tr><td align="center" rowspan="1" colspan="1"> AH </td><td align="center" rowspan="1" colspan="1"> 785.67 (182.50) </td></tr><tr><td align="center" rowspan="1" colspan="1"> AO </td><td align="center" rowspan="1" colspan="1"> 445.33 (102.00) </td></tr><tr><td align="center" rowspan="1" colspan="1"> HA </td><td align="center" rowspan="1" colspan="1"> 556.67 (50.35) </td></tr><tr><td colspan="3" rowspan="1"><hr></hr></td></tr><tr><td rowspan="4" align="center" colspan="1"><bold>1 week</bold></td><td align="center" rowspan="1" colspan="1"> B </td><td align="center" rowspan="1" colspan="1"> 601.00 (18.50) </td></tr><tr><td align="center" rowspan="1" colspan="1"> AH </td><td align="center" rowspan="1" colspan="1"> 817.67 (133.30) </td></tr><tr><td align="center" rowspan="1" colspan="1"> AO </td><td align="center" rowspan="1" colspan="1"> 1147.33 (470.82) </td></tr><tr><td align="center" rowspan="1" colspan="1"> HA </td><td align="center" rowspan="1" colspan="1"> 999.33 (86.11) </td></tr></tbody></table><table-wrap-foot><fn><p>B = blasted titanium;</p><p>AH = alkali and heat treated;</p><p>AO = anodic oxidized;</p><p>HA = hydroxyapatite coated.</p></fn></table-wrap-foot></table-wrap></sec><sec sec-type="discussion"><title>DISCUSSION</title><p>Laminin has been identified as one of the proteins being attached on biomaterial
surfaces after the implantation process, and has been proposed to participate in
osteoblast adhesion on biomaterials [<xref ref-type="bibr" rid="B22">22</xref>].
However, its biological role has not been studied compared to other important bone
related proteins [<xref ref-type="bibr" rid="B39">39</xref>]. Previous <italic>in vitro</italic>studies have identified the integrin subunit β1 as a mechanism involved in
human osteoblast adhesion [<xref ref-type="bibr" rid="B27">27</xref>], and have
suggested that laminin-1 recruits osteoprogenitor cells through an attachment effect
[<xref ref-type="bibr" rid="B25">25</xref>,<xref ref-type="bibr" rid="B26">26</xref>]. Nevertheless, none of those studies has investigated the ability of
laminin to precipitate on different titanium surfaces or its potential to
precipitate CaP.</p><p>The results from this study showed that the Ca/P ratio was higher for the possibly
bioactive surfaces after 1 and 24 h as compared to blasted titanium surfaces. The
ability of the possibly bioactive surfaces to induce a higher calcium phosphate
level at the initial incubation phase declined by time and no difference in the
ratio was observed after one week of incubation. These findings are in agreement
with the results presented by Stenport et al. [<xref ref-type="bibr" rid="B40">40</xref>]. However, it is important to keep in mind that the control blasted
group had not been subjected to any surface modification leading to possibly
bioactive properties which may explain why neither calcium nor phosphate were
detectable prior to incubation or after one hour of incubation. Thus, the more rapid
response of the possibly bioactive surfaces could be explained by the ability of
initial crystals of calcium and phosphorous to promote further calcium phosphate
precipitation, a process known as crystal growth [<xref ref-type="bibr" rid="B19">19</xref>]. Hence, the Ca/P ratios illustrated in <xref ref-type="fig" rid="fig6">Figure 6</xref> include the sum of the calcium and phosphate
originating in the surface treatment, and the crystals having precipitated during
the SBF incubation. Interestingly, at 72 h and 1 week the Ca/P ratio was
approximately 1.67, which corresponds to hydroxyapatite formation, and indicates
that the formed CaP can be identified as hydroxyapatite.</p><p>Previously performed studies examining the nucleation rate of calcium phosphate in
SBF solution including BSA have not always examined the topography of the tested
surfaces [<xref ref-type="bibr" rid="B18">18</xref>,<xref ref-type="bibr" rid="B20">20</xref>,<xref ref-type="bibr" rid="B41">41</xref>]. In our study, we have
examined three surface roughness parameters of the tested surfaces according to the
norms for a complete topographic analysis [<xref ref-type="bibr" rid="B38">38</xref>]. All three tested parameters, S<sub>a</sub>, S<sub>ds</sub> and S<sub>dr</sub>,
increased for all tested surfaces with incubation time, indicating a rougher surface
created by the calcium phosphate precipitation. This finding is in agreement with
the SEM observation.</p><p>In an earlier SBF study with four titanium surfaces claimed to be bioactive, i.e.
fluoride etched, alkali and heat treated, anodically oxidated and hydroxyapatite
coated, the evaluation of the BSA precipitation on surfaces was performed by
counting the amount of nitrogen on the surfaces as an indirect way of protein
detection. It was concluded that modified surfaces possessed a more rapid BSA
precipitation compared to the blasted surfaces [<xref ref-type="bibr" rid="B40">40</xref>]. In the present study, we have labelled laminin with iodine-125,
which detected the amount of protein more directly. Zeng et al. [<xref ref-type="bibr" rid="B21">21</xref>] compared BSA precipitation on
hydroxyapatite, fluorapatite and pure titanium surfaces, and found that different
surface composition and structure influenced the adsorption of BSA. The results of
the present study demonstrated the ability of laminin to equally precipitate on
various titanium surfaces within the first hour of incubation regardless of the
underlying surface topography or chemistry. This finding suggests that laminin
possesses the ability to precipitate easily on biomaterial surfaces.</p><p>All tested surfaces induced higher CaP precipitation when incubated in SBF containing
laminin with a concentration equivalent to the human blood plasma as compared to
blasted surfaces solely incubated in SBF [<xref ref-type="bibr" rid="B36">36</xref>]. A possible mechanism for laminin promoting CaP precipitation may be its
function as a nucleation center. 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="B42">42</xref>]. Some of the domains exposed from this protein conformation may act
as nucleation centers for calcium ions thereby increasing the local calcium
phosphate 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="B43">43</xref>]. Hence, it is possible that the enhanced
calcium phosphate formation observed in this study triggers osteoblast
differentiation around laminin coated implants also when applied <italic>in
vivo</italic>, acting as a complementary mechanism to the osteoblast activation
by the integrin β1 subunit. An additional advantage of the possible function of
laminin as nucleation center is its possible incorporation within the calcium
phosphates. Hence, the proposed model would provide beneficial sustaining of laminin
by leading to lower clearance, and higher local concentration for a longer period of
time, thereby leading to prolonged stimulation of the surrounding osteoblasts.</p><p>Nevertheless, despite the interesting findings from this study one has to keep in
mind that <italic>in vivo</italic> protein interactions are more complex. Therefore
more <italic>in vitro</italic> and <italic>in vivo</italic> studies are required in order to clarify
the role of laminin in the interaction of biomaterials with the host bone
tissue.</p></sec><sec sec-type="conclusions"><title>CONCLUSIONS</title><p>The results of the present study demonstrate the potential of laminin to equally
precipitate on titanium surfaces subjected to various surface modifications, and to
enhance apatite formation on blasted titanium surfaces when compared to blasted
surfaces incubated in simulated body fluid in the absence of laminin. Among the
tested surface modifications, alkali and heat treatment seemed to induce more rapid
CaP precipitation. The findings of this study are intriguing since laminin may
function as a nucleation center, thus locally elevating the calcium concentration,
thereby having a positive effect on osteoblast differentiation. Nevertheless, since
the <italic>in vivo</italic> protein interactions are more complex, further studies
are required in order to clarify the role of laminin in the interaction of
biomaterials with the host bone tissue.</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 help with protein labeling. 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
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