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Inicio Boletín de la Sociedad Española de Cerámica y Vidrio Enhancing bone tissue regeneration with rGO-coated Si-Ca-P bioceramic scaffold
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Enhancing bone tissue regeneration with rGO-coated Si-Ca-P bioceramic scaffold
Potenciación de la regeneración ósea a través de una biocerámica de Si-Ca-P recubierta con grafeno reducido
Patricia Mazóna,
Corresponding author
pmazon@umh.es

Corresponding author.
, Jeevithan Elangob, José Eduardo Maté-Sánchez de Valb, Piedad N. De Azaa
a Instituto de Bioingeniería, Universidad Miguel Hernández, Avda. Universidad s/n, Elche, 03202 Alicante, Spain
b Department of Biomaterials Engineering, Faculty of Health Sciences, UCAM-Universidad Católica San Antonio de Murcia, Guadalupe, 30107 Murcia, Spain
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Biomaterials demand has been growing exponentially in the last few decades&#46; Trauma injuries and increasing life expectancy mainly&#44; have focused many attention on designing and implementing scaffolds for bone tissue repair and bone replacement&#46; Bone tissue&#44; once damaged or necrotic&#44; does not possess sufficient regeneration ability in order to undergo self-repair&#44; because of nonvascular and cell-free characteristics&#46; Suitable scaffold materials could be implemented to accelerate the growth and differentiation of bone cells <a class="elsevierStyleCrossRef" href="#bib0355">&#91;1&#93;</a>&#46; In the last decades&#44; there is a great variety of synthetic materials that are developed as scaffolds&#44; such as synthetic polymers&#44; ceramics&#44; and metals&#46; However&#44; their ability to repair bone tissue continues being less than that of autologous bone grafts and allogenic bone grafts do it&#46; Nevertheless&#44; availability for autologous ones&#44; and immunogenic response for allogenic ones are problematic&#46; In another hand&#44; synthetic scaffolds presented disadvantages as compatibility&#44; toxicity&#44; anticoagulant properties&#44; lack of adequate mechanical properties&#44; etc&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Ceramic-based bone graft substitutes such as hydroxyapatite &#40;HA&#41;&#44; &#946;-tricalcium phosphate &#40;&#946;-TCP&#41;&#44; and bioactive glasses have been widely studied for bone tissue engineering&#44; particularly for bone repair&#44; due to their biocompatibility and osteoconductivity <a class="elsevierStyleCrossRef" href="#bib0360">&#91;2&#93;</a>&#46; Also&#44; the incorporation of ions as Si&#44; Mg&#44; or Zn into their chemical compositions could improve stem cells proliferation when they are seeded on the materials&#44; and their differentiation into osteoblastic cells <a class="elsevierStyleCrossRef" href="#bib0365">&#91;3&#93;</a>&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Graphene and its derivatives possess remarkable properties that are currently being extensively researched in various fields&#44; including gene therapy&#44; bioelectronics&#44; and tissue engineering&#46; These materials have a large surface area&#44; high strength and flexibility&#44; and the ability to adapt to irregular surfaces&#44; as well as exceptional thermal and electrical conductivity and optical properties&#46; The aromatic structure&#39;s planar carbon&#8211;carbon bonds generate free &#960; electrons and reactive sites&#44; which make surface functionalization a straightforward process <a class="elsevierStyleCrossRefs" href="#bib0370">&#91;4&#44;5&#93;</a>&#46; Moreover&#44; they have demonstrated the ability to induce stem cells to differentiate into specific tissue cells and regulate cell interactions&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">Mechanical properties of bioceramics in bone tissue engineering could be improved by combination with graphene derivatives&#44; without hampering their structures or biocompatibilities <a class="elsevierStyleCrossRef" href="#bib0380">&#91;6&#93;</a>&#46; Furthermore&#44; several studies have shown how graphene and its derivatives can strongly promote cell adhesion <a class="elsevierStyleCrossRef" href="#bib0385">&#91;7&#93;</a>&#44; by enhance cellular adherence&#44; proliferation&#44; and osteoblast differentiation <a class="elsevierStyleCrossRef" href="#bib0390">&#91;8&#93;</a>&#44; and how the high elastic modulus of graphene-based materials can promote spontaneous osteoblastic differentiation <a class="elsevierStyleCrossRef" href="#bib0395">&#91;9&#93;</a>&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Reduced graphene oxide &#40;rGO&#41; is a derivative of graphene obtained through chemical or thermal reduction of graphene oxide &#40;GO&#41;&#46; rGO is characterized by having a lower number of oxygenated groups&#44; which enables the creation of defects in the atomic structure that favor interaction with biomolecules&#44; cells and polymers <a class="elsevierStyleCrossRef" href="#bib0400">&#91;10&#93;</a>&#46; Because of that&#44; rGO combined a structural similarity to pristine graphene &#40;high surface area and strength&#41; <a class="elsevierStyleCrossRefs" href="#bib0405">&#91;11&#44;12&#93;</a>&#44; and on the contrary to GO&#44; presents highly conductivity <a class="elsevierStyleCrossRef" href="#bib0415">&#91;13&#93;</a> and moderate dispersibility in water <a class="elsevierStyleCrossRefs" href="#bib0420">&#91;14&#44;15&#93;</a>&#46; However&#44; there are still oxygen functional groups in rGO for functionalization&#44; and the amount of that could be controlled via different reduction techniques&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Previously&#44; we reported that mesenquimal stem cells &#40;MSCs&#41; isolated from adult human bone marrow &#40;ahMSCs&#41; were able to successfully grow and adhere on TCP&#44; Si-TCP and Si-Ca-P ceramics <a class="elsevierStyleCrossRefs" href="#bib0430">&#91;16&#8211;18&#93;</a>&#46; This study aimed to enhance the functionality of a bioceramic scaffold composed of Si-Ca-P by optimizing its surface properties through the application of a thin layer of reduced graphene oxide &#40;rGO&#41;&#46; The goal was to achieve complete coverage of the scaffold with a uniform layer of rGO&#44; in order to improve its biocompatibility and promote the growth and differentiation of stem cells&#46; Also&#44; we determined its in vitro osteogenic potential&#44; in order to know the mechanisms by which reduced graphene induces osteoblastic differentiation&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Materials</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Synthesis and characterization of the ceramic as base material for the scaffold</span><p id="par0035" class="elsevierStylePara elsevierViewall">The starting ceramic material&#44; Nurse&#39;s A-phase ceramic &#40;from now and beyond named as SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span>&#41;&#44; was prepared through a solid-state reaction method from a stoichiometric mixture of calcium hydrogen phosphate anhydrous &#40;CaHPO<span class="elsevierStyleInf">4</span>&#59; Panreac S&#46;L&#46;U&#46;&#44; Barcelona&#44; Spain&#41;&#44; calcium carbonate &#40;CaCO<span class="elsevierStyleInf">3</span><span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>99&#46;0<span class="elsevierStyleHsp" style=""></span>wt&#37;&#59; Fluka-Sigma Aldrich Quimica SL&#44; Madrid&#44; Spain&#41; with an average particle size of 13&#46;8<span class="elsevierStyleHsp" style=""></span>&#956;m&#44; and silicon oxide &#40;SiO<span class="elsevierStyleInf">2</span><span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>99&#46;7<span class="elsevierStyleHsp" style=""></span>wt&#37;&#59; Strem Chemicals UK Ltd&#44; Cambridge&#44; UK&#41; with an average particle size<span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>50<span class="elsevierStyleHsp" style=""></span>&#956;m&#46; Discs-shaped SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> samples&#44; measuring 7<span class="elsevierStyleHsp" style=""></span>mm in diameter and 3<span class="elsevierStyleHsp" style=""></span>mm in thickness&#44; were cut from the sintered bulk with a diamond saw&#46; For more information on the technique and the ceramic&#39;s characterization&#44; please refer to a previous publication <a class="elsevierStyleCrossRef" href="#bib0445">&#91;19&#93;</a>&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">The ground sample in this study was subjected to mineralogical characterization by X-ray Diffraction&#44; XRD &#40;Bruker-AXS D8 Advance&#44; Karksruhe&#44; Germany&#41;&#44; using CuK<span class="elsevierStyleInf">&#945;1&#44;2</span> radiation &#40;1&#46;54056<span class="elsevierStyleHsp" style=""></span>&#8491;&#41; and operating at 40<span class="elsevierStyleHsp" style=""></span>kV at 30<span class="elsevierStyleHsp" style=""></span>mA and compared with the data base provide by Joint Committee on Powered Diffraction Standards &#40;JCPDS&#41;&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">The material&#39;s microstructure was analyzed using Scanning Electron Microscopy&#44; SEM &#40;SEM-Hitachi S-3500N&#44; Ibaraki&#44; Japan&#41; using an accelerating voltage of 20<span class="elsevierStyleHsp" style=""></span>kV&#46; Chemical composition analysis was conducted by fitting the scanning electron microscope with an energy dispersive X-ray spectroscopy&#44; EDS system &#40;INCA system by Oxford Instrument Analytical&#44; UK&#41;&#46; Prior to SEM-EDS observations&#44; the samples were coated with palladium&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">The porosity and pore size distribution for SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic was analyzed by mercury porosimetry using a Poremaster-60 GT &#40;Quantachrome Instrument&#44; Boyton Beach&#44; FL&#41; within the pressure range of 5&#46;395&#8211;410785<span class="elsevierStyleHsp" style=""></span>kPa&#44; which corresponds to a pore diameter range between 300 and 0&#46;0035<span class="elsevierStyleHsp" style=""></span>&#956;m&#46; Three samples were analyzed using this technique&#46; An additional sample was used in each case if the obtained porosity values differed by more than 5&#37;&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Reduced graphene coating of ceramic base material for scaffold</span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Reduced graphene coating of SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic preparation</span><p id="par0055" class="elsevierStylePara elsevierViewall">To apply the GO coating to the SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic discs&#44; the discs were immersed in 50<span class="elsevierStyleHsp" style=""></span>ml of aqueous GO suspensions &#40;GRAPHENEA&#44; San Sebastian&#44; Spain&#41; with a concentration of 0&#46;5<span class="elsevierStyleHsp" style=""></span>mg&#47;ml for five cycles of 10<span class="elsevierStyleHsp" style=""></span>min&#44; followed by 10-min drying periods at 100<span class="elsevierStyleHsp" style=""></span>&#176;C between each cycle&#46; After this&#44; the GO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> samples were dried overnight at 100<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; Subsequently&#44; the GO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> samples were immersed in an aqueous solution of ascorbic acid &#40;20<span class="elsevierStyleHsp" style=""></span>mM&#41; at 70<span class="elsevierStyleHsp" style=""></span>&#176;C for 3<span class="elsevierStyleHsp" style=""></span>h&#44; using the method proposed by Fern&#225;ndez-Merino et al&#46; <a class="elsevierStyleCrossRef" href="#bib0450">&#91;20&#93;</a>&#44; to reduce the GO&#46; The reduced graphene oxide-coated SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> &#40;rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span>&#41; scaffolds were washed with distilled H<span class="elsevierStyleInf">2</span>O and dried at 37<span class="elsevierStyleHsp" style=""></span>&#176;C&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffolds were individually packaged and sterilized by gas-plasma &#40;Sterrad-1005TM&#44; ASP Irvine&#44; Ca&#46;&#41;&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Characterization of reduced graphene coated-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold</span><p id="par0065" class="elsevierStylePara elsevierViewall">Mineralogical characterization of rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffolds were evaluated from powder by XRD&#44; following the same protocol described for ceramic starting material for uncoated samples&#44; and results were compared with these ones&#46; The surface morphology was characterized by SEM-EDS as described for uncoated material&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">The chemical structure for coated sample was studied with X-ray photoelectron spectroscopy&#44; XPS Spectroscopy &#40;K-Alpha&#44; Thermo-Scientific&#41; from powder of the samples&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Porosity and pore size distribution of scaffold were analyzed&#44; in the same way as starting ceramic&#44; by mercury porosimetry for comparative purpose&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">In vitro bioactivity of the reduced graphene coated-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold</span><p id="par0080" class="elsevierStylePara elsevierViewall">An in vitro bioactivity study was conducted to assess the calcium phosphate capability induction by immersing the scaffolds in an acellular simulated body fluid &#40;SBF&#41;&#44; according to the Standard ISO&#47;FDIS 23317&#58;2014 <a class="elsevierStyleCrossRef" href="#bib0455">&#91;21&#93;</a>&#46; The scaffolds were positioned inside containers made of polystyrene and filled with 50<span class="elsevierStyleHsp" style=""></span>ml of SBF&#44; which had an ion plasma concentration similar to that of human blood plasma at pH 7&#46;40&#46; Next&#44; the containers with the SBF and samples were placed in a shaking water bath and incubated at 37<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; After different periods of immersion&#44; which ranged up to 14 days&#44; the specimens were taken out&#44; rinsed with deionized water&#44; and air-dry at room temperature&#46; In order to examine the surfaces of the specimens after being exposed to SBF&#44; they were coated with palladium and subjected to surface analysis using SEM and microanalysis with EDS&#46; At specific immersion intervals&#44; the SBF was collected and its calcium&#44; silicon&#44; and phosphorus ion concentrations were analyzed using inductively coupled plasma optical emission spectrometry &#40;ICP-OES PerkinElmer Optima 2000&#41;&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">Finally&#44; in order to know the chemical bond composition of the new precipitated layer&#44; Fourier Transform Infrared Spectrometry with Attenuated Total Reflectance accessory&#44; ATR&#8211;FTIR &#40;Thermo Scientific Nicolet iS5 equipped with an iDR ATR accessory&#41; was used&#46;</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Cell culture</span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">In vitro cell culture</span><p id="par0090" class="elsevierStylePara elsevierViewall">ahMSCs &#40;ATCC PCS-500-012&#8482;&#41; were purchased from LGC GmbH&#44; Louis-Pasteur&#44; Luckenwalde&#44; Germany and were used to evaluate the biocompatibility of SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold&#46; In brief&#44; the cells were cultured as per the standard cell culture protocol using complete mesenchymal stem cells basal medium with the required supplements as per the LGC GmbH instruction&#46; The cells with complete medium were cultured in a 5&#37; CO<span class="elsevierStyleInf">2</span> incubator at 37<span class="elsevierStyleHsp" style=""></span>&#176;C until confluence&#44; followed by sub-culture&#46; The cells with passage n&#176; 4&#8211;7 were used for the biocompatibility experiments&#46; Every time&#44; the cells were trypsinized using 0&#46;25&#37; trypsin&#47;EDTA as they were adhered on top of the samples&#44; and then quantified using an automated Invitrogen cell counter &#40;Invitrogen&#44; Carlsbad&#44; CA&#44; USA&#41;&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Cell proliferation</span><p id="par0095" class="elsevierStylePara elsevierViewall">Before cell culture&#44; samples were sterilized overnight under UV by using a UV Sterilizer&#44; 9W&#44; 60<span class="elsevierStyleHsp" style=""></span>Hz &#40;SKU&#58; OT-HSYXF-2624-EU&#44; model YM-9002&#44; China&#41;&#46; The sterilized samples were transferred into 48 well culture plates and ahMSCs with a cell density of 5<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">4</span> were seeded on top of the samples&#46; The cells without test samples were considered as control&#46; The cells were allowed to grow for 7 days and then the total number of grown cells was counted by automated cell counter &#40;Invitrogen&#41;&#46; The percentage of cells proliferation of tested samples was calculated by comparing control group&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Cell cytotoxicity</span><p id="par0100" class="elsevierStylePara elsevierViewall">The cytotoxic effect of SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold were determined by MTT Assay Protocol as per our previous protocol <a class="elsevierStyleCrossRef" href="#bib0460">&#91;22&#93;</a>&#46; In brief&#44; the ahMSCs were seeded onto the top of the samples at a density of 5<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">4</span> cells in 48 well culture plates as described earlier&#44; and the positive control cells were seeded without any sample&#46; The ahMSCs with SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> were allowed to culture for 7 days before MTT treatment&#46; 50<span class="elsevierStyleHsp" style=""></span>&#956;l of MTT reagent with a concentration of 5<span class="elsevierStyleHsp" style=""></span>mg&#47;ml phosphate buffer saline &#40;PBS&#41; was added in each well along with culture medium for 3<span class="elsevierStyleHsp" style=""></span>h&#46; Then&#44; the wells were gently washed with PBS twice and the formazan crystals were solubilized with DMSO at 37<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; 5&#37; CO<span class="elsevierStyleInf">2</span> for 15<span class="elsevierStyleHsp" style=""></span>min&#46; Then 100<span class="elsevierStyleHsp" style=""></span>&#956;l of solubilized formazan crystals were transferred to a transparent-flat-bottom 96-well plate and the absorbance was recorded at 570<span class="elsevierStyleHsp" style=""></span>nm in a SpectraMAX Id3 plate reader&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Cell loading ability</span><p id="par0105" class="elsevierStylePara elsevierViewall">In order to evaluate the total capacity of cells that can adhere on top of the SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> samples&#44; we have done the cell loading ability as per our earlier protocol <a class="elsevierStyleCrossRef" href="#bib0460">&#91;22&#93;</a>&#46; Briefly&#44; the ahMSCs with a cell density of 1<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">5</span> were seeded on top of the samples as described earlier&#46; After 6<span class="elsevierStyleHsp" style=""></span>h of cell seeding&#44; the samples were transferred to new 48 well plate in order to quantify the exact cell number that have been attached on top of the samples&#46; At the same time&#44; the cells attached other than bioactive ceramic SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> samples in 48-well plates were also quantified for comparison&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Cell adhesion behavior on SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> by scanning electron microscopy</span><p id="par0110" class="elsevierStylePara elsevierViewall">To investigate the cell adhesion behavior&#44; the ahMSCs were seeded with a cell density of 5<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">4</span> on all the SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> samples and cultured for 3 and 7 days&#46; After 7 days&#8217; culture&#44; the cells were gently washed with PBS and were fixed with 2&#46;5&#37; glutaraldehyde for 1<span class="elsevierStyleHsp" style=""></span>d&#44; followed by consecutive fixing with 4&#37; paraformaldehyde for a day&#46; The samples were briefly washed with PBS after each fixation&#44; and the samples were dehydrated with increased ethanol concentration &#40;serial dilutions&#41; starting from 10&#44; 25&#44; 50&#44; 75 and 100&#37; ethanol &#40;30<span class="elsevierStyleHsp" style=""></span>min&#46; in each dehydration&#41;&#46; After dehydration the samples were briefly air dried for the analysis by SEM&#46;</p></span></span></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Results</span><p id="par0115" class="elsevierStylePara elsevierViewall">Mineralogical characterization by XRD of uncoated and coated samples &#40;SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span>&#41; is shown in <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#46; Each diffraction peak for starting ceramic &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>a&#41; was identified as the characteristic reflection of Nurse&#39;s A phase &#40;JCPDS card n&#176; 11-0676&#41; indicated on figure by an asterisk &#40;&#42;&#41;&#46; A slight displacement from the corresponding JCPDS card&#44; about 0&#46;1&#176;&#44; was observed for diffraction peaks&#44; due to solid solution&#46; Any significant differences were observed for the reduced graphene coated sample by this method &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>b&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0120" class="elsevierStylePara elsevierViewall">The XPS survey spectra &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>a&#41; and the information included in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> were use to describe elemental composition of SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold&#46; Notable differences were found related with calcium&#44; silicon and phosphorous small content in rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold&#44; and as well in the biggest content in carbon that it presents&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0125" class="elsevierStylePara elsevierViewall">In the C1s XPS spectra &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>b&#41;&#44; four distinct peaks can be discerned at 284&#46;56<span class="elsevierStyleHsp" style=""></span>eV &#40;C<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>C sp2&#41;&#44; 286&#46;40<span class="elsevierStyleHsp" style=""></span>eV &#40;C<span class="elsevierStyleGlyphsbnd"></span>C sp3&#41;&#44; 285&#46;46<span class="elsevierStyleHsp" style=""></span>eV &#40;C<span class="elsevierStyleGlyphsbnd"></span>OH&#41; and 288&#46;14<span class="elsevierStyleHsp" style=""></span>eV &#40;O<span class="elsevierStyleGlyphsbnd"></span>C<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>C&#41;&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">SEM was used to examine the microstructure of the rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; It could be clearly observed rGO-sheet covering the entire ceramic disk with a thickness about 2<span class="elsevierStyleHsp" style=""></span>&#956;m&#44; and a gap between both&#46; For rGO sheet an irregular surface was observed&#44; as it was expected&#44; while the ceramic showed a granular microstructure&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0135" class="elsevierStylePara elsevierViewall">Microporosity level and its distribution were studied by mercury porosimetry for SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>&#41;&#46; With increasing pressure&#44; mercury infiltrated the progressively smaller pores&#46; As expected no large difference was observed for both samples related to intra- and interparticle porosity&#46; Summarized results for porosimetry analyzed are presented in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a> for a better comprehension&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0140" class="elsevierStylePara elsevierViewall">In a previous study&#44; in vitro bioactivity of SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic was investigated <a class="elsevierStyleCrossRef" href="#bib0465">&#91;23&#93;</a>&#46; In order to determine changes in the bioactivity of the rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold&#44; its bioactivity was assessed following immersion in SBF for different periods of time&#46; Surface morphology was evaluated by SEM-EDS after each immersion interval&#46; The results after soaking for 1&#44; 5 and 7 days are shown in <a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>a&#8211;c&#46; After 1 day soaking time in SBF&#44; only rGO sheet morphology was observed with any evidence of bioactivity &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>a&#41;&#44; while after 5 days &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>b&#41; a small and disperse globular precipitate was observed over rGO sheet&#44; that increased in sized covering the entire surface after 7 days &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>c&#41;&#46; Precipitated layer was identified as hydroxyapatite &#40;HA&#41;-like by SEM-EDS microanalysis&#44; with a Ca&#47;P ratio on average &#8764;2&#46;6&#46; This ratio&#44; higher than the one HA stoichiometric presents&#44; suggests a carbonate-hydroxyapatite &#40;CHA&#41; is growing on the surface of scaffold&#46;</p><elsevierMultimedia ident="fig0025"></elsevierMultimedia><p id="par0145" class="elsevierStylePara elsevierViewall">Once saturation on the surface of the scaffolds was confirmed&#44; a longer experiment was conducted to analyze the precipitate layer in depth&#44; with a maximum soaking time of 14 days&#46; The precipitate layer was examined by SEM cross-section analysis&#44; as shown in <a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>d&#46; To determine the thickness of the precipitate on the scaffold&#44; SEM measurements were taken by recording 20 measurements per sample in triplicate&#46; The precipitate layer was continuous with a thickness value reaching 8&#46;6<span class="elsevierStyleHsp" style=""></span>&#956;m&#46; A gap between the precipitated layer and reduced graphene sheet was observed due to vacuum use in SEM technique&#44; additionally to the one between reduced graphene sheet and ceramic&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">ICP-OES was used to analyze the changes in ion concentrations &#40;calcium&#44; phosphorus&#44; and silicon&#41; from the SBF over different immersion periods&#46; These results are presented in <a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>&#46; Calcium concentration increased until day 5 of SBF soaking as the silicon one&#44; which indicate an initial dissolution of the material previous to precipitate formation on the surface&#46; As the HA-like precipitate grows thicker&#44; some dissolution continues to occur&#44; although it becomes more difficult as a result of the ion diffusion through the newly formed HA-like phase&#44; and into the surrounding medium&#46;</p><elsevierMultimedia ident="fig0030"></elsevierMultimedia><p id="par0155" class="elsevierStylePara elsevierViewall">An ATR&#8211;FTIR analysis of the new precipitate layer was performed to confirmed the apatite type growing over the scaffold &#40;<a class="elsevierStyleCrossRef" href="#fig0035">Fig&#46; 7</a>&#41;&#46; It could be observed absorptions corresponding to phosphate and silicate groups &#40;overlapped in 1016&#44; 942 and 869<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleSup">&#8722;1</span>&#41;&#44; and phosphate groups in 601&#44; 548<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleSup">&#8722;1</span>&#46; In addition&#44; infrared spectra showed bands related to the presence of OH<span class="elsevierStyleSup">&#8722;</span> groups centered at 3396<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleSup">&#8722;1</span> and 1638<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleSup">&#8722;1</span>&#44; and as well bands corresponding to CO<span class="elsevierStyleInf">3</span><span class="elsevierStyleSup">2&#8722;</span> groups at 1467<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleSup">&#8722;1</span> and 1402<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleSup">&#8722;1</span>&#44; confirming the presence of CHA because of the partial substitution of the phosphate groups in the HA-like crystalline structure <a class="elsevierStyleCrossRef" href="#bib0470">&#91;24&#93;</a>&#46;</p><elsevierMultimedia ident="fig0035"></elsevierMultimedia><p id="par0160" class="elsevierStylePara elsevierViewall">One of the main properties of biomaterials in order to be biocompatible is their effect in cells proliferation&#46; Therefore&#44; the effect of uncoated and coated samples in ahMSCs proliferation was assessed by culturing ahMSCs on SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold for 7 days&#46; Interestingly&#44; the cells cultured on both samples showed a rate of proliferation greater compared to the control &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0040">Fig&#46; 8</a>a&#41;&#46; However&#44; there was no significant changes observed associated to the reduced graphene coating&#46;</p><elsevierMultimedia ident="fig0040"></elsevierMultimedia><p id="par0165" class="elsevierStylePara elsevierViewall">The cytotoxic results &#40;<a class="elsevierStyleCrossRef" href="#fig0040">Fig&#46; 8</a>b&#41; showed that the cells cultured on ceramic SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold had significantly higher OD value at 570<span class="elsevierStyleHsp" style=""></span>nm compared to control &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46; Reduced graphene coated scaffold had slightly higher OD value&#44; however&#44; the differences were insignificant&#46; Interestingly&#44; the cells cultured on studied samples had 2 folds higher rate of compatibility compared to control cells&#44; which is in agreement with the cell proliferation study &#40;<a class="elsevierStyleCrossRef" href="#fig0040">Fig&#46; 8</a>a&#41;&#46;</p><p id="par0170" class="elsevierStylePara elsevierViewall">The cell loading ability was determined by seeding ahMSCs with a cell density of 1<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">5</span> cells per sample &#40;<a class="elsevierStyleCrossRef" href="#fig0045">Fig&#46; 9</a>&#41;&#46; After 6<span class="elsevierStyleHsp" style=""></span>h of incubation&#44; the capacity of uncoated and coated samples was in general lower than control group &#40;cells without ceramic in 2D culture&#41;&#44; however the difference was insignificant&#46; Loading capacity of ahMSCs was lower in rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold from SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic&#46;</p><elsevierMultimedia ident="fig0045"></elsevierMultimedia><p id="par0175" class="elsevierStylePara elsevierViewall">The cell adhesion behavior of ahMSCs on uncoated and coated samples was determined on 3 and 7 days by SEM analysis of surface&#39;s morphology &#40;<a class="elsevierStyleCrossRef" href="#fig0050">Fig&#46; 10</a>&#41;&#46; In general&#44; it had good ahMSCs adhesion&#44; and cells were grown with more interconnected filaments penetrated in many directions&#46; As expected&#44; the number of cells spreading was higher in day 7 compared to day 3 and more in rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold than SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic&#46; Interestingly&#44; the surface of rGO coated scaffold was completed covered by ahMSCs with more flat-shape cells through filament-like interconnection throughout surface&#44; which directly claimed the biocompatibility of rGO coated SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold for culturing ahMSCs&#46;</p><elsevierMultimedia ident="fig0050"></elsevierMultimedia></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Discussion</span><p id="par0180" class="elsevierStylePara elsevierViewall">In the last decades the search of an appropriate scaffold for tissue engineering has focused a lot of attention&#46; For this aim&#44; bioceramics such as calcium phosphate have shown good properties due to their mineralogical structure close to the natural bone&#44; even more when they include ions such as silicon in their composition <a class="elsevierStyleCrossRefs" href="#bib0475">&#91;25&#44;26&#93;</a>&#46; Nurse&#39;s A phase &#40;SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic&#41; has shown to be an excellent scaffold for tissue repair by studies developed in our laboratory <a class="elsevierStyleCrossRef" href="#bib0485">&#91;27&#93;</a>&#44; although it would be possible to improve their mechanical strength and osteoconductivity&#46;</p><p id="par0185" class="elsevierStylePara elsevierViewall">Graphene derivatives interactions with living organisms for regenerative medicine&#44; have been extensively research&#44; focusing specially on GO and rGO&#44; confirming their biocompatibility <a class="elsevierStyleCrossRefs" href="#bib0490">&#91;28&#8211;31&#93;</a>&#46; Their unique two-dimensional structure and biological interface behavior <a class="elsevierStyleCrossRef" href="#bib0510">&#91;32&#93;</a>&#44; together with their excellent osteogenesis inducing capability&#44; make GO and rGO highly promising materials for use as scaffolds in bone tissue engineering&#44; collaborating with biomaterials such as HA&#44; calcium silicate&#44; chitosan and 45S5Bioglass&#174; between others <a class="elsevierStyleCrossRefs" href="#bib0515">&#91;33&#8211;37&#93;</a>&#46;</p><p id="par0190" class="elsevierStylePara elsevierViewall">In order to improve biological properties in this study SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic was uniformly coated with reduced graphene oxide as a way to supplying large surface area&#44; high reactivity and biocompatibility <a class="elsevierStyleCrossRefs" href="#bib0410">&#91;12&#44;38&#93;</a>&#46; The reduction of GO to rGO removes partially oxygen-containing functional groups and restores the sp2 structure&#44; resulting in an increase in conductivity <a class="elsevierStyleCrossRef" href="#bib0545">&#91;39&#93;</a>&#46; This improved conductivity is beneficial for the creation of a suitable signal conduction between cells and scaffolds&#44; which is important for many tissue engineering applications <a class="elsevierStyleCrossRef" href="#bib0550">&#91;40&#93;</a>&#46;</p><p id="par0195" class="elsevierStylePara elsevierViewall">Solid-state reaction was used to prepare the starting ceramic material&#44; that was then uniformly coated with rGO&#46; Mineralogical characterization of coated and uncoated samples by XRD &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41; indicated a monophasic composition concordant with the phase diagram Ca<span class="elsevierStyleInf">2</span>SiO<span class="elsevierStyleInf">4</span><span class="elsevierStyleGlyphsbnd"></span>Ca<span class="elsevierStyleInf">3</span>&#40;PO<span class="elsevierStyleInf">4</span>&#41;<span class="elsevierStyleInf">2</span><a class="elsevierStyleCrossRef" href="#bib0555">&#91;41&#93;</a>&#44; corresponding to a solid solution of Nurse&#39;s A phase &#40;SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span>&#41;&#44; checked by the JCPDS data base&#46; Any significant differences in diffraction peaks were observed after coating &#40;rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span>&#41;&#46;</p><p id="par0200" class="elsevierStylePara elsevierViewall">In order to describe the elemental composition of scaffold&#44; XPS analysis was realized from rGO surface and SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; As expected rGO surface present small quantities of calcium&#44; silicon and phosphorous&#44; that are present in the ceramic structure below the coating&#46; A bigger quantitative percentage of carbon &#40;C1s&#41; is observed in rGO coating&#44; up to 97&#46;09&#37; &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The presence of rGO coating was confirmed by the deconvolution bands concerning to C<span class="elsevierStyleGlyphdbnd"></span>C sp2 and C<span class="elsevierStyleGlyphsbnd"></span>C sp3 hybridation&#44; and also two deconvolution bands corresponding to hydroxyl groups C<span class="elsevierStyleGlyphsbnd"></span>OH and carboxylate groups O<span class="elsevierStyleGlyphsbnd"></span>C<span class="elsevierStyleGlyphdbnd"></span>O&#44; according to literature <a class="elsevierStyleCrossRefs" href="#bib0500">&#91;30&#44;42&#93;</a>&#46;</p><p id="par0205" class="elsevierStylePara elsevierViewall">Morphological analysis of the rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold was realized by SEM &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; It showed a uniform and continuous coating of the SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic disk with a sheet of rGO&#44; presenting a clear gap between the granular ceramic structure and the rGO sheet&#46; The rough and undulating surface of rGO can provide physical stimulation that promotes cell adhesion&#44; proliferation&#44; and differentiation&#46; The high surface area of rGO also provides more binding sites for osteoinductive factors&#44; which can enhance osteogenic differentiation of the cells&#46; Additionally&#44; the &#960;&#8211;&#960; stacking and hydrogen bonding interactions of rGO can facilitate the adsorption and release of osteoinductive factors by non-covalent binding&#44; further promoting osteogenesis <a class="elsevierStyleCrossRef" href="#bib0565">&#91;43&#93;</a>&#46;</p><p id="par0210" class="elsevierStylePara elsevierViewall">Mercury porosimetry is a technique used to determine the pore structure of porous materials by measuring the penetration of mercury into the pores under increasing pressure&#46; By analyzing the data&#44; one can obtain information about the pore size distribution&#44; porosity&#44; and specific surface area of the material&#46; In the case of this study&#44; it was used to compare the microporosity of the coated and uncoated ceramic samples&#46; Minor difference were observed for both samples&#44; that presents two main absorptions in a similar way between 186 and 2<span class="elsevierStyleHsp" style=""></span>&#956;m&#44; slightly lower for rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> &#40;continuous line in <a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>a&#41;&#46; These absorptions correspond to intense peaks in the differential volume centered between 8 and 2<span class="elsevierStyleHsp" style=""></span>&#956;m &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>b&#41;&#46; The initial absorptions observed can be attributed to the filling of interparticle gaps&#44; whereas the subsequent ones are likely caused by the filling of intraparticle voids&#46; According to literature pore structures&#44; because of the presence of larger surface areas&#44; play a crucial role in enhancing the interaction between implanted material and natural bone&#44; which can lead to an increase in protein absorption&#44; ion exchange and bone-like apatite formation <a class="elsevierStyleCrossRef" href="#bib0570">&#91;44&#93;</a>&#46; Any significant difference in porosity and density measures were found for uncoated and coated ceramic &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#44; but a bigger intraparticle porosity was observed for rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold &#40;16&#46;48&#37;&#41; while it was 11&#46;43&#37; for uncoated ceramic&#46; However&#44; according to literature a surface increment and biocompatibility is expected due to rGO coating&#46;</p><p id="par0215" class="elsevierStylePara elsevierViewall">Scaffold&#39;s bioactivity was studied in vitro according to Standard ISO&#47;FDIS 23317&#58;2014 <a class="elsevierStyleCrossRef" href="#bib0455">&#91;21&#93;</a>&#44; reflecting the ability to stimulate calcium phosphate precipitate formation through immersion in SBF for 1&#44; 5 and 7 days &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>a&#8211;c&#41;&#46; After 1 day soaking no indication of bioactivity was found on the scaffold&#39;s surface&#44; but it appeared at 5 days&#44; when some isolated spheres and some groups of them were found on the surface&#46; The surface appeared completely covered with a precipitate layer after 7 days of soaking in SBF&#44; appearing even some cracking because of the vacuum used by SEM analysis&#46; Extending the time of immersion in SBF until 14 days and realizing cross-section analysis &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>d&#41;&#44; a uniform and continuous precipitate layer was observed above the rGO coating sheet&#44; reaching thickness of 8&#46;6<span class="elsevierStyleHsp" style=""></span>&#956;m&#46; Results obtained for this potential scaffold presents no significate differences in bioactivity rate and grade from SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic&#44; previously studied in our laboratory <a class="elsevierStyleCrossRef" href="#bib0465">&#91;23&#93;</a>&#46;</p><p id="par0220" class="elsevierStylePara elsevierViewall">The concentrations of silicon&#44; calcium and phosphorus ion released were measured using ICP-OES after different immersion times in SBF &#40;<a class="elsevierStyleCrossRef" href="#fig0030">Fig&#46; 6</a>&#41;&#46; Initial composition of SBF is included in results as 0 days soaking time&#46; It was observed an increment in Ca and Si ion concentration until day 5 of soaking&#44; which it is correlated with an initial dissolution of the ceramic prior to reaction with serum&#46; After that time dissolution seems to be present at the same time HA-like precipitate layer is growing on the surface of scaffold&#44; what difficult the ion diffusion processes across these layer&#46;</p><p id="par0225" class="elsevierStylePara elsevierViewall">Chemical composition of new precipitate layer&#44; with a Ca&#47;P ratio of 2&#46;6 measured by EDS&#44; was analyzed by ATR&#8211;FTIR &#40;<a class="elsevierStyleCrossRef" href="#fig0035">Fig&#46; 7</a>&#41;&#46; In addition to absorptions corresponding to phosphate and silicate groups by means of serum used in bioactivity assay&#44; absorption bands of hydroxyl and carbonate groups led us to confirm the presence of a CHA phase&#46; This apatite deficient in calcium is partially substituted with silicon from the physiologic medium&#46;</p><p id="par0230" class="elsevierStylePara elsevierViewall">Scaffolds based on rGO have demonstrated their ability to promote cell proliferation and differentiation by enhancing cell-scaffold and cell-cell interactions through a variety of cellular signals&#44; such as chemical or electrical signals <a class="elsevierStyleCrossRef" href="#bib0575">&#91;45&#93;</a>&#46; This can be attributed to the unique properties of rGO&#44; including its high surface area&#44; excellent mechanical and electrical properties&#44; high biocompatibility&#44; and ability to promote cell adhesion and proliferation <a class="elsevierStyleCrossRefs" href="#bib0580">&#91;46&#8211;50&#93;</a>&#46; Additionally&#44; the tunable properties of scaffolds incorporating rGO offers advantages such as improving hydrophilicity&#44; mechanical strength&#44; protein adsorption and stability&#44; cell adhesion&#44; proliferation&#44; and enhancing electrical properties of the scaffolds <a class="elsevierStyleCrossRefs" href="#bib0605">&#91;51&#8211;54&#93;</a>&#46; These properties make them potentially useful in tissue engineering and regenerative medicine applications&#44; providing an optimal environment for cells to adhere and proliferate <a class="elsevierStyleCrossRef" href="#bib0625">&#91;55&#93;</a>&#46;</p><p id="par0235" class="elsevierStylePara elsevierViewall">The in vitro cell culture study confirmed that the SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold increased the ahMSCs proliferation rate than control &#40;<a class="elsevierStyleCrossRef" href="#fig0040">Fig&#46; 8</a>a&#41;&#44; which ultimately proved the efficiency of these samples on tissue engineering application&#46; It is well known that the biomaterials which stimulate the proliferation rate of biological cells directly claim the biocompatibility in practical application&#46; The present study results of in vitro cell cultures were in total agreement with literature <a class="elsevierStyleCrossRefs" href="#bib0630">&#91;56&#8211;59&#93;</a>&#46;</p><p id="par0240" class="elsevierStylePara elsevierViewall">Furthermore&#44; rGO has shown a higher capability in electron transferring which may be effective in accelerating differentiation <a class="elsevierStyleCrossRef" href="#bib0650">&#91;60&#93;</a>&#44; specially adipogenesis and osteogenesis through an improvement in the adsorption of differentiation factors and cell adhesion <a class="elsevierStyleCrossRef" href="#bib0655">&#91;61&#93;</a>&#44; and it is suggested as more compatible <a class="elsevierStyleCrossRefs" href="#bib0660">&#91;62&#8211;64&#93;</a>&#46; As well&#44; some studies have suggested that rGO may induce the production of reactive oxygen species and activate specific signaling pathways that promote angiogenesis <a class="elsevierStyleCrossRef" href="#bib0675">&#91;65&#93;</a>&#46;</p><p id="par0245" class="elsevierStylePara elsevierViewall">There are studies that have been shown cytotoxicity when rGO is used&#44; because of some variation in physical properties derived from the method of synthesis&#46; Regarding cytotoxicity&#44; it could be influence for dose&#44; surface charge or lateral size <a class="elsevierStyleCrossRefs" href="#bib0680">&#91;66&#44;67&#93;</a>&#44; however&#44; in this study any sign of cytotoxicity was found &#40;<a class="elsevierStyleCrossRef" href="#fig0040">Fig&#46; 8</a>b&#41;&#46;</p><p id="par0250" class="elsevierStylePara elsevierViewall">Regarding to cell loading ability &#40;<a class="elsevierStyleCrossRef" href="#fig0045">Fig&#46; 9</a>&#41;&#44; ahMSCs loading capacity of rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> was slightly lower than SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> one&#46;</p><p id="par0255" class="elsevierStylePara elsevierViewall">The morphological changes of ahMSCs seeded on bioactive samples after 3 and 7 days were determined by SEM &#40;<a class="elsevierStyleCrossRef" href="#fig0050">Fig&#46; 10</a>&#41;&#46; It was observed adhesion and growing for cells with interconnected filaments extending over the surface&#46; It is worth mentioning that rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold appeared completely cover of cells after 7 days what confirmed a better environment for growing and proliferation cells expected after rGO coating&#46;</p><p id="par0260" class="elsevierStylePara elsevierViewall">Another advantage reported for scaffolds&#8217; rGO incorporation is the excellent mechanical properties <a class="elsevierStyleCrossRefs" href="#bib0690">&#91;68&#8211;70&#93;</a>&#46; Mechanical properties will be presented in further studies&#46;</p></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Conclusion</span><p id="par0265" class="elsevierStylePara elsevierViewall">The developed scaffold combines a calcium silicophosphate ceramic that provide a mineralogical composition similar to natural bone&#44; with an rGO coating&#46; Although both have proven their excellent in vitro bioactivity&#44; rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold has shown an increasing osteoconductivity capability by inherent &#960;&#8211;&#960; conjugation&#44; with any toxic effect in ahMSCs&#46; The compatibility of the scaffold has been proved with good cell adherent properties&#44; which would allow its use as potential scaffold for application in the future bone regenerative medicine</p></span></span>"
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          "titulo" => "Introduction"
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          "titulo" => "Materials"
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              "identificador" => "sec0015"
              "titulo" => "Synthesis and characterization of the ceramic as base material for the scaffold"
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              "titulo" => "Reduced graphene coating of ceramic base material for scaffold"
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                  "titulo" => "Reduced graphene coating of SiCaPO ceramic preparation"
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                  "titulo" => "Characterization of reduced graphene coated-SiCaPO scaffold"
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                2 => array:2 [
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                  "titulo" => "In vitro bioactivity of the reduced graphene coated-SiCaPO scaffold"
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              "titulo" => "Cell culture"
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                  "titulo" => "In vitro cell culture"
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                  "titulo" => "Cell proliferation"
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                  "titulo" => "Cell cytotoxicity"
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                  "titulo" => "Cell loading ability"
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                  "titulo" => "Cell adhesion behavior on SiCaPO by scanning electron microscopy"
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          "titulo" => "Results"
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          "titulo" => "Discussion"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Ceramic-based bone graft substitutes have been extensively studied for bone tissue engineering&#44; due to their biocompatibility and osteoconductivity&#46; Additionally&#44; several studies have shown how graphene and its derivatives&#44; due to their unique properties&#44; can strongly promote cell adhesion&#44; by enhance cellular adherence&#44; proliferation&#44; and osteoblast differentiation&#44; and how graphene-based materials can promote spontaneous osteoblastic differentiation&#46; The aim of this study was the use of a calcium silicophosphate ceramic&#44; previously prepared in our laboratory&#44; that presents excellent in vitro bioactivity&#44; optimizing its operation by rGO coating&#46; After coating with rGO any significant differences were observed in diffraction peaks from starting calcium silicophosphate ceramic&#44; and SEM analysis showed a rough and undulating surface that favored a high specific surface area for promoting cell adhesion&#44; proliferation and differentiation of cells&#46; It could be confirmed by in vitro cell cultured with ahMSCs&#44; showing adhesion and growing for cells with interconnected filaments extending over the surface&#44; covering it after 7 days&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Los sustitutos cer&#225;micos para injertos &#243;seos han sido estudiados ampliamente en ingenier&#237;a de tejidos debido a su biocompatibilidad y osteoconductividad&#46; Adem&#225;s&#44; varios estudios han demostrado c&#243;mo el grafeno y sus derivados&#44; por sus propiedades &#250;nicas&#44; pueden favorecer activamente la adhesi&#243;n celular al mejorar la adherencia celular&#44; la proliferaci&#243;n y la diferenciaci&#243;n de osteoblastos&#44; y c&#243;mo los biomateriales basados en grafeno pueden promover la diferenciaci&#243;n osteobl&#225;stica espont&#225;nea&#46; El objetivo de este estudio fue el uso de una cer&#225;mica de silicofosfato de calcio&#44; previamente preparada en nuestro laboratorio&#44; que presenta excelente bioactividad <span class="elsevierStyleItalic">in vitro&#44;</span> optimizando su funcionamiento por recubrimiento con grafeno reducido&#46; Tras el recubrimiento con rGO no se observaron diferencias significativas en los picos de difracci&#243;n de la cer&#225;mica de silicofosfato de calcio de partida&#44; y el an&#225;lisis SEM mostr&#243; una superficie rugosa y ondulada que favorec&#237;a una superficie espec&#237;fica alta para promover la adhesi&#243;n celular&#44; la proliferaci&#243;n y la diferenciaci&#243;n de las c&#233;lulas&#46; Este hecho fue confirmado mediante cultivo celular <span class="elsevierStyleItalic">in vitro</span> con ahMSCs&#44; observ&#225;ndose adhesi&#243;n y crecimiento de c&#233;lulas con filamentos interconectados que se extend&#237;an sobre la superficie&#44; cubri&#233;ndola completamente tras 7 d&#237;as&#46;</p></span>"
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">&#40;a&#41; Cumulative curve vs pore diameter and &#40;b&#41; differential volume for SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic &#40;dotted line&#41; and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold &#40;continuous line&#41;&#46;</p>"
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          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">SEM images of the rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold&#39;s surface morphology after soaking time in SBF for &#40;a&#41; 1 day &#40;b&#41; 5 days&#44; &#40;c&#41; 7 days&#44; and &#40;d&#41; cross-section images&#44; after soaking time in SBF for 14 days&#46;</p>"
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          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">ICP-OES analysis for changes in SBF ion concentration&#44; after different soaking times&#46;</p>"
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          "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">ATR&#8211;FTIR spectra from the precipitate layer of the 14 days SBF soaked scaffold&#46;</p>"
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      7 => array:7 [
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          "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">&#40;a&#41; Proliferation cells on SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold&#44; and &#40;b&#41; Cytotoxicity study for SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold&#46;</p>"
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          "en" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Cell loading ability for SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold&#46;</p>"
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          "en" => "<p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Cell morphological characteristics of ahMSCs cultured on bioactive ceramics for 3 and 7 days for C&#58; SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> and G&#58; rGO-coated SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span>&#46;</p>"
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                  <table border="0" frame="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37; Atoms&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">C1s&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Ca2p3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Si2p3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">P2p3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">48&#46;12&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">35&#46;3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">12&#46;3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">4&#46;29&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t\ttop\n
                  \t\t\t\t">rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">97&#46;09&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t">1&#46;79&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">1&#46;01&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;11&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Interparticle porosity &#40;&#37;&#41;<span class="elsevierStyleSup">b</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Theoretical porosity &#40;&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">1&#46;5530&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">47&#46;2147&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;1311&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">11&#46;4397&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">35&#46;7749&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">47&#46;2092&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">43&#46;9816&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;1251&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t">16&#46;4825&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">27&#46;4992&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">43&#46;9816&nbsp;\t\t\t\t\t\t\n
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          "en" => "<p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Porosity and density results for SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> ceramic and rGO-SiCaP<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">5</span> scaffold&#46;</p>"
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      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
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        0 => array:2 [
          "identificador" => "bibs0015"
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            0 => array:3 [
              "identificador" => "bib0355"
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Promising graphene-based nanomaterials and their biomedical applications and potential risks&#58; a comprehensive review"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "J&#46; Li"
                            1 => "H&#46; Zeng"
                            2 => "Z&#46; Zeng"
                            3 => "Y&#46; Zeng"
                            4 => "T&#46; Xie"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1021/acsbiomaterials.1c00875"
                      "Revista" => array:6 [
                        "tituloSerie" => "ACS Biomater&#46; Sci&#46; Eng&#46;"
                        "fecha" => "2021"
                        "volumen" => "7"
                        "paginaInicial" => "5363"
                        "paginaFinal" => "5396"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/34747591"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            1 => array:3 [
              "identificador" => "bib0360"
              "etiqueta" => "&#91;2&#93;"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Mechanism of in vitro reaction of a new scaffold ceramic similar to porous bone"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:4 [
                            0 => "A&#46; D&#237;az-Arca"
                            1 => "P&#46; Velasquez"
                            2 => "P&#46; Maz&#243;n"
                            3 => "P&#46;N&#46; De Aza"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.jeurceramsoc.2020.01.045"
                      "Revista" => array:5 [
                        "tituloSerie" => "J&#46; Eur&#46; Ceram&#46; Soc&#46;"
                        "fecha" => "2020"
                        "volumen" => "40"
                        "paginaInicial" => "2200"
                        "paginaFinal" => "2206"
                      ]
                    ]
                  ]
                ]
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