Validating cone-beam computed tomography for peri-implant bone morphometric analysis
Identifieur interne : 000816 ( Pmc/Corpus ); précédent : 000815; suivant : 000817Validating cone-beam computed tomography for peri-implant bone morphometric analysis
Auteurs : Yan Huang ; Jeroen Van Dessel ; Maarten Depypere ; Mostafa Ezeldeen ; Alexandru Andrei Iliescu ; Emanuela Dos Santos ; Ivo Lambrichts ; Xin Liang ; Reinhilde JacobsSource :
- Bone Research [ 2095-4700 ] ; 2014.
Abstract
Cone-beam computed tomography (CBCT) has been recently used to analyse trabecular bone structure around dental implants. To validate the use of CBCT for three-dimensional (3D) peri-implant trabecular bone morphometry by comparing it to two-dimensional (2D) histology, 36 alveolar bone samples (with implants
Url:
DOI: 10.1038/boneres.2014.10
PubMed: 26273522
PubMed Central: 4472132
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Validating cone-beam computed tomography for peri-implant bone morphometric analysis</title><author><name sortKey="Huang, Yan" sort="Huang, Yan" uniqKey="Huang Y" first="Yan" last="Huang">Yan Huang</name><affiliation><nlm:aff id="aff1"><institution>OMFS IMPATH Research Group, Department of Imaging & Pathology, Faculty of Medicine, University of Leuven and Oral & Maxillofacial Surgery, University Hospitals Leuven</institution>, Leuven,<country>Belgium</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>State Key Laboratory of Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff></affiliation></author><author><name sortKey="Dessel, Jeroen Van" sort="Dessel, Jeroen Van" uniqKey="Dessel J" first="Jeroen Van" last="Dessel">Jeroen Van Dessel</name><affiliation><nlm:aff id="aff1"><institution>OMFS IMPATH Research Group, Department of Imaging & Pathology, Faculty of Medicine, University of Leuven and Oral & Maxillofacial Surgery, University Hospitals Leuven</institution>, Leuven,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Depypere, Maarten" sort="Depypere, Maarten" uniqKey="Depypere M" first="Maarten" last="Depypere">Maarten Depypere</name><affiliation><nlm:aff id="aff3"><institution>ESAT/PSI, Medical Image Computing, KU Leuven</institution>, Leuven,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Ezeldeen, Mostafa" sort="Ezeldeen, Mostafa" uniqKey="Ezeldeen M" first="Mostafa" last="Ezeldeen">Mostafa Ezeldeen</name><affiliation><nlm:aff id="aff1"><institution>OMFS IMPATH Research Group, Department of Imaging & Pathology, Faculty of Medicine, University of Leuven and Oral & Maxillofacial Surgery, University Hospitals Leuven</institution>, Leuven,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Iliescu, Alexandru Andrei" sort="Iliescu, Alexandru Andrei" uniqKey="Iliescu A" first="Alexandru Andrei" last="Iliescu">Alexandru Andrei Iliescu</name><affiliation><nlm:aff id="aff4"><institution>Faculty of Dentistry, UMF Craiova</institution>,<country>Romania</country></nlm:aff></affiliation></author><author><name sortKey="Santos, Emanuela Dos" sort="Santos, Emanuela Dos" uniqKey="Santos E" first="Emanuela Dos" last="Santos">Emanuela Dos Santos</name><affiliation><nlm:aff id="aff5"><institution>School of Dentistry, Pontifical Catholic University of Paraná</institution>, Curitiba,<country>Brazil</country></nlm:aff></affiliation></author><author><name sortKey="Lambrichts, Ivo" sort="Lambrichts, Ivo" uniqKey="Lambrichts I" first="Ivo" last="Lambrichts">Ivo Lambrichts</name><affiliation><nlm:aff id="aff6"><institution>Biomedical Research Institute, Hasselt University</institution>, Diepenbeek,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Liang, Xin" sort="Liang, Xin" uniqKey="Liang X" first="Xin" last="Liang">Xin Liang</name><affiliation><nlm:aff id="aff7"><institution>School of Stomatology, Dalian Medical University</institution>, Dalian,<country>China</country></nlm:aff></affiliation></author><author><name sortKey="Jacobs, Reinhilde" sort="Jacobs, Reinhilde" uniqKey="Jacobs R" first="Reinhilde" last="Jacobs">Reinhilde Jacobs</name><affiliation><nlm:aff id="aff1"><institution>OMFS IMPATH Research Group, Department of Imaging & Pathology, Faculty of Medicine, University of Leuven and Oral & Maxillofacial Surgery, University Hospitals Leuven</institution>, Leuven,<country>Belgium</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26273522</idno><idno type="pmc">4472132</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4472132</idno><idno type="RBID">PMC:4472132</idno><idno type="doi">10.1038/boneres.2014.10</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000816</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000816</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Validating cone-beam computed tomography for peri-implant bone morphometric analysis</title><author><name sortKey="Huang, Yan" sort="Huang, Yan" uniqKey="Huang Y" first="Yan" last="Huang">Yan Huang</name><affiliation><nlm:aff id="aff1"><institution>OMFS IMPATH Research Group, Department of Imaging & Pathology, Faculty of Medicine, University of Leuven and Oral & Maxillofacial Surgery, University Hospitals Leuven</institution>, Leuven,<country>Belgium</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>State Key Laboratory of Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff></affiliation></author><author><name sortKey="Dessel, Jeroen Van" sort="Dessel, Jeroen Van" uniqKey="Dessel J" first="Jeroen Van" last="Dessel">Jeroen Van Dessel</name><affiliation><nlm:aff id="aff1"><institution>OMFS IMPATH Research Group, Department of Imaging & Pathology, Faculty of Medicine, University of Leuven and Oral & Maxillofacial Surgery, University Hospitals Leuven</institution>, Leuven,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Depypere, Maarten" sort="Depypere, Maarten" uniqKey="Depypere M" first="Maarten" last="Depypere">Maarten Depypere</name><affiliation><nlm:aff id="aff3"><institution>ESAT/PSI, Medical Image Computing, KU Leuven</institution>, Leuven,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Ezeldeen, Mostafa" sort="Ezeldeen, Mostafa" uniqKey="Ezeldeen M" first="Mostafa" last="Ezeldeen">Mostafa Ezeldeen</name><affiliation><nlm:aff id="aff1"><institution>OMFS IMPATH Research Group, Department of Imaging & Pathology, Faculty of Medicine, University of Leuven and Oral & Maxillofacial Surgery, University Hospitals Leuven</institution>, Leuven,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Iliescu, Alexandru Andrei" sort="Iliescu, Alexandru Andrei" uniqKey="Iliescu A" first="Alexandru Andrei" last="Iliescu">Alexandru Andrei Iliescu</name><affiliation><nlm:aff id="aff4"><institution>Faculty of Dentistry, UMF Craiova</institution>,<country>Romania</country></nlm:aff></affiliation></author><author><name sortKey="Santos, Emanuela Dos" sort="Santos, Emanuela Dos" uniqKey="Santos E" first="Emanuela Dos" last="Santos">Emanuela Dos Santos</name><affiliation><nlm:aff id="aff5"><institution>School of Dentistry, Pontifical Catholic University of Paraná</institution>, Curitiba,<country>Brazil</country></nlm:aff></affiliation></author><author><name sortKey="Lambrichts, Ivo" sort="Lambrichts, Ivo" uniqKey="Lambrichts I" first="Ivo" last="Lambrichts">Ivo Lambrichts</name><affiliation><nlm:aff id="aff6"><institution>Biomedical Research Institute, Hasselt University</institution>, Diepenbeek,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Liang, Xin" sort="Liang, Xin" uniqKey="Liang X" first="Xin" last="Liang">Xin Liang</name><affiliation><nlm:aff id="aff7"><institution>School of Stomatology, Dalian Medical University</institution>, Dalian,<country>China</country></nlm:aff></affiliation></author><author><name sortKey="Jacobs, Reinhilde" sort="Jacobs, Reinhilde" uniqKey="Jacobs R" first="Reinhilde" last="Jacobs">Reinhilde Jacobs</name><affiliation><nlm:aff id="aff1"><institution>OMFS IMPATH Research Group, Department of Imaging & Pathology, Faculty of Medicine, University of Leuven and Oral & Maxillofacial Surgery, University Hospitals Leuven</institution>, Leuven,<country>Belgium</country></nlm:aff></affiliation></author></analytic><series><title level="j">Bone Research</title><idno type="ISSN">2095-4700</idno><idno type="eISSN">2095-6231</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Cone-beam computed tomography (CBCT) has been recently used to analyse trabecular bone structure around dental implants. To validate the use of CBCT for three-dimensional (3D) peri-implant trabecular bone morphometry by comparing it to two-dimensional (2D) histology, 36 alveolar bone samples (with implants <italic>n</italic>=27 <italic>vs.</italic> without implants <italic>n</italic>=9) from six mongrel dogs, were scanned <italic>ex vivo</italic> using a high-resolution (80 µm) CBCT. After scanning, all samples were decalcified and then sectioned into thin histological sections (∼6 μm) to obtain high contrast 2D images. By using CTAn imaging software, bone morphometric parameters including trabecular number (Tb.N), thickness (Tb.Th), separation (Tb.Sp) and bone volume fraction (BV/TV) were examined on both CBCT and corresponding histological images. Higher Tb.Th and Tb.Sp, lower BV/TV and Tb.N were found on CBCT images (<italic>P</italic><0.001). Both measurements on the peri-implant trabecular bone structure showed moderate to high correlation (<italic>r</italic>=0.65–0.85). The Bland–Altman plots showed strongest agreement for Tb.Th followed by Tb.Sp, Tb.N and BV/TV, regardless of the presence of implants. The current findings support the assumption that peri-implant trabecular bone structures based on high-resolution CBCT measurements are representative for the underlying histological bone characteristics, indicating a potential clinical diagnostic use of CBCT-based peri-implant bone morphometric characterisation.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Bone Res</journal-id><journal-id journal-id-type="iso-abbrev">Bone Res</journal-id><journal-title-group><journal-title>Bone Research</journal-title></journal-title-group><issn pub-type="ppub">2095-4700</issn><issn pub-type="epub">2095-6231</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26273522</article-id><article-id pub-id-type="pmc">4472132</article-id><article-id pub-id-type="pii">boneres201410</article-id><article-id pub-id-type="doi">10.1038/boneres.2014.10</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Validating cone-beam computed tomography for peri-implant bone morphometric analysis</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Huang</surname><given-names>Yan</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Dessel</surname><given-names>Jeroen Van</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Depypere</surname><given-names>Maarten</given-names></name><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>EzEldeen</surname><given-names>Mostafa</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Iliescu</surname><given-names>Alexandru Andrei</given-names></name><xref ref-type="aff" rid="aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Santos</surname><given-names>Emanuela Dos</given-names></name><xref ref-type="aff" rid="aff5">5</xref></contrib><contrib contrib-type="author"><name><surname>Lambrichts</surname><given-names>Ivo</given-names></name><xref ref-type="aff" rid="aff6">6</xref></contrib><contrib contrib-type="author"><name><surname>Liang</surname><given-names>Xin</given-names></name><xref ref-type="aff" rid="aff7">7</xref></contrib><contrib contrib-type="author"><name><surname>Jacobs</surname><given-names>Reinhilde</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="corresp" rid="caf1">*</xref></contrib><aff id="aff1"><label>1</label><institution>OMFS IMPATH Research Group, Department of Imaging & Pathology, Faculty of Medicine, University of Leuven and Oral & Maxillofacial Surgery, University Hospitals Leuven</institution>, Leuven,<country>Belgium</country></aff><aff id="aff2"><label>2</label><institution>State Key Laboratory of Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></aff><aff id="aff3"><label>3</label><institution>ESAT/PSI, Medical Image Computing, KU Leuven</institution>, Leuven,<country>Belgium</country></aff><aff id="aff4"><label>4</label><institution>Faculty of Dentistry, UMF Craiova</institution>,<country>Romania</country></aff><aff id="aff5"><label>5</label><institution>School of Dentistry, Pontifical Catholic University of Paraná</institution>, Curitiba,<country>Brazil</country></aff><aff id="aff6"><label>6</label><institution>Biomedical Research Institute, Hasselt University</institution>, Diepenbeek,<country>Belgium</country></aff><aff id="aff7"><label>7</label><institution>School of Stomatology, Dalian Medical University</institution>, Dalian,<country>China</country></aff></contrib-group><author-notes><corresp id="caf1"><label>*</label><email>reinhilde.jacobs@med.kuleuven.be</email></corresp></author-notes><pub-date pub-type="epub"><day>10</day><month>06</month><year>2014</year></pub-date><pub-date pub-type="collection"><year>2014</year></pub-date><volume>2</volume><fpage>14010</fpage><lpage></lpage><history><date date-type="received"><day>15</day><month>02</month><year>2014</year></date><date date-type="rev-recd"><day>05</day><month>04</month><year>2014</year></date><date date-type="accepted"><day>21</day><month>04</month><year>2014</year></date></history><permissions><copyright-statement>Copyright © 2014 Sichuan University</copyright-statement><copyright-year>2014</copyright-year><copyright-holder>Sichuan University</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <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></license-p></license></permissions><abstract><p>Cone-beam computed tomography (CBCT) has been recently used to analyse trabecular bone structure around dental implants. To validate the use of CBCT for three-dimensional (3D) peri-implant trabecular bone morphometry by comparing it to two-dimensional (2D) histology, 36 alveolar bone samples (with implants <italic>n</italic>=27 <italic>vs.</italic> without implants <italic>n</italic>=9) from six mongrel dogs, were scanned <italic>ex vivo</italic> using a high-resolution (80 µm) CBCT. After scanning, all samples were decalcified and then sectioned into thin histological sections (∼6 μm) to obtain high contrast 2D images. By using CTAn imaging software, bone morphometric parameters including trabecular number (Tb.N), thickness (Tb.Th), separation (Tb.Sp) and bone volume fraction (BV/TV) were examined on both CBCT and corresponding histological images. Higher Tb.Th and Tb.Sp, lower BV/TV and Tb.N were found on CBCT images (<italic>P</italic><0.001). Both measurements on the peri-implant trabecular bone structure showed moderate to high correlation (<italic>r</italic>=0.65–0.85). The Bland–Altman plots showed strongest agreement for Tb.Th followed by Tb.Sp, Tb.N and BV/TV, regardless of the presence of implants. The current findings support the assumption that peri-implant trabecular bone structures based on high-resolution CBCT measurements are representative for the underlying histological bone characteristics, indicating a potential clinical diagnostic use of CBCT-based peri-implant bone morphometric characterisation.</p></abstract></article-meta></front><body><sec><title>Introduction</title><p>Bone quality, which is a significant determinant of the survival rate of an implant,<sup><xref ref-type="bibr" rid="bib1">1</xref>,<xref ref-type="bibr" rid="bib2">2</xref></sup> depends on the bone mineral density as well as the spatial structure of trabecular bone.<sup><xref ref-type="bibr" rid="bib3">3</xref>,<xref ref-type="bibr" rid="bib4">4</xref></sup> To determine the internal structural properties of peri-implant trabeculae, a proper quantitative morphometry with the imaging resolution superior to trabecular dimensions is desirable.<sup><xref ref-type="bibr" rid="bib5">5</xref></sup></p><p>Conventionally, bone structure could be assessed <italic>in vitro</italic> by histomorphometry. This approach remains the gold standard due to its high spatial resolution and image contrast, though it is time-consuming and destructive for secondary measurements.<sup><xref ref-type="bibr" rid="bib6">6</xref></sup> Another alternate technique to quantify bone structure <italic>in vitro</italic> is micro-computed tomography (micro-CT), which has been mainly applied in small animal bones and bone biopsies. <italic>In vivo</italic> imaging of trabecular bone structure is feasible using high-resolution magnetic resonance imaging and multislice CT,<sup><xref ref-type="bibr" rid="bib7">7</xref>,<xref ref-type="bibr" rid="bib8">8</xref></sup> but these are limited by metal artefacts (MRI/CT) or abundant radiation exposure (CT). In contrast, cone-beam computed tomography (CBCT), as an easily available clinical imaging modality developed since the late 1990s,<sup><xref ref-type="bibr" rid="bib9">9</xref>,<xref ref-type="bibr" rid="bib10">10</xref></sup> offers an efficient non-invasive scanning in combination with higher spatial resolution, reduced radiation dose and scan costs.<sup><xref ref-type="bibr" rid="bib11">11</xref>,<xref ref-type="bibr" rid="bib12">12</xref></sup></p><p>The value of CBCT in clinical practice has been largely demonstrated in oral and maxillofacial pathology, surgery and implantology,<sup><xref ref-type="bibr" rid="bib13">13</xref></sup> mainly focusing on bone density and linear bone measurements.<sup><xref ref-type="bibr" rid="bib14">14</xref></sup> Only a few studies described the use of CBCT for trabecular bone structure assessment.<sup><xref ref-type="bibr" rid="bib12">12</xref>,<xref ref-type="bibr" rid="bib15">15</xref>,<xref ref-type="bibr" rid="bib16">16</xref></sup> Recently, this imaging modality was utilized in a pilot study for analysing peri-implant trabecular bone morphology, suggesting that the latest CBCT equipment with a resolution of 80 µm may probably serve as a three-dimensional (3D) imaging modality for the clinical assessment of the anisotropic trabecular microstructures.<sup><xref ref-type="bibr" rid="bib17">17</xref></sup> To date, CBCT for bone morphometric evaluation has been validated with other imaging acquisition modalities such as micro-CT<sup><xref ref-type="bibr" rid="bib18">18</xref></sup> or conventional CT<sup><xref ref-type="bibr" rid="bib19">19</xref></sup> in human cadavers, further indicating the possibility of quantifying and monitoring changes of trabecular bone microarchitecture <italic>in vivo</italic> using CBCT. However, less is known about the effectiveness and accuracy of CBCT in comparison to histomorphometry, which will actually add to understanding of previous 3D findings, and help to explain the mechanical behavior of bones. In addition, whether the existence of metal implants could influence the bone morphometry quantification by using CBCT has hardly been documented.</p><p>Therefore, the aim of this study was to verify the accuracy of high-resolution CBCT in peri-implant trabecular bone structure analyses using histology as a reference.</p></sec><sec><title>Materials and methods</title><sec><title>Samples</title><p>The current samples consisted of 27 alveolar bone biopsies with custom-made implants and 9 alveolar bone biopsies without the implants (natural healing after teeth extraction, <xref rid="tbl1" ref-type="table">Table 1</xref>) retrieved from six mongrel dogs (male, weight 14.8–18.1 kg, age 20–24 months old). The detail of biopsies were outlined in a previous study.<sup><xref ref-type="bibr" rid="bib17">17</xref></sup> Briefly, all dogs were sacrificed by means of an intravenous injection of an overdose 0.1 mL⋅kg<sup>−1</sup> Xylazine Hydrochloride (Changchun Military Academy of Medical Sciences, Changchun, China). The jawbones were dissected and defleshed. Then, each implant was removed with a careful preservation of 3−5 mm peri-implant bone as one piece of sample. The experiment protocol was in accordance with the ethical guidelines of KU Leuven (P059-2012-TK).</p></sec><sec><title>CBCT image acquisition</title><p>All the bone samples were scanned using a high resolution CBCT (Accuitomo 170; Morita, Kyoto, Japan). The exposition and reconstruction parameters for the scan were as following: 0.08 mm voxel size, 360° rotation, ∼950 projections, 90 kV tube voltage, 2.0 mA tube current, 30.8 s scanning time, 40×40 mm field of view, CsI-aSi flat panel detector and 43 (lower jaw)–54 (upper jaw) μSv effective dose.<sup><xref ref-type="bibr" rid="bib20">20</xref></sup> To prevent any movement during the scanning process, each sample was mounted vertically into a sponge block, with the long axis of the implant perpendicular to the scanning beam. The calibration of CBCT imager was performed by the manufacturer before the radiographic study.</p><p>The original CBCT data were reconstructed as 3D images by CTAn V1.11 software (CTAnalyser; Skyscan, Antwerp, Belgium). Three ring-shaped volumes of interest (VOIs) were automatically selected in a distance of 1 mm away from the surface of the implant, at coronal, middle and apical sections along the axis of the implant as indicated in <xref ref-type="fig" rid="fig1">Figure 1a</xref>. All three VOIs were selected through intermediate cross sections by using a custom processing in the CTAn V1.11 by an experienced observer (JVD). Binary regions of interest (ROIs) were further generated by a custom processing algorithm based on adaptive thresholding segmentation,<sup><xref ref-type="bibr" rid="bib17">17</xref></sup> excluding implant and cortical bone; trabecular morphometric parameters were then calculated based on this binary segmentation of trabecular bone (<xref ref-type="fig" rid="fig1">Figure 1b</xref>).</p></sec><sec><title>Histology</title><p>After CBCT analysis, the samples were decalcified in 0.5 mmol⋅L<sup>−1</sup> EDTA phosphate buffered saline (pH 7.4) at 4 °C for 10 months. The implants were then removed from the specimens using surgical forceps. Followed by the dehydration and embedding in paraffin, thin serial sections (∼6 μm) were sectioned along the mesial–distal direction in the middle of the implant or extraction area, where more trabecular bone could be observed. Three serial sections in the most central cut area, corresponding to the greatest dimensions of the samples in length and diameter, were selected and stained with the trichrome Masson stain.</p><p>Digital microscopic images of two-dimensional (2D) histological sections were captured by an automated and calibrated camera (Nikon Eclipse 80i; Nikon Co., Tokyo, Japan) and then transferred to grey-level images. The grey-level images were transformed to binary images, enabling a clear separation of trabecular bone and bone marrow (ImageJ, NIH, Maryland, USA). Similar ROIs in the mesial–distal plane, as previously defined in the CBCT measurements, were manually selected by one trained observer (EDS) independently (<xref ref-type="fig" rid="fig1">Figure 1c and 1d</xref>). Those selected ROIs were then exported as BMP images and imported into trabecular bone analysis software CTAn for a semi-automatic 2D histomorphometry. Three serial sections per sample were selected to conduct this 2D histomorphometry. Then the results from coronal, middle and apical levels were averaged. All observations were guaranteed to use a standard PC (Intel Pentium Dual-Core, CPU at 3.20 GHz, 4 GB of RAM and a 64-bit operating system) with a 17-inch LCD monitor (Dell, Austin, TX, USA).</p></sec><sec><title>Morphometric analysis</title><p>CBCT provided measurements obtained directly from reconstructed images based on consecutive 2D images. Only those 3D morphometric parameters that could be compared with 2D histomorphometric measurements were selected for this study. Therefore, 2D and 3D parameters of trabecular bone architecture, as commonly used and directly measured indicators,<sup><xref ref-type="bibr" rid="bib21">21</xref></sup> were quantified from CBCT images (VOIs) and histological images (ROIs) using 3D and 2D imaging processing in CTAn, respectively, following the recommendations of the American Society of Bone and Mineral Metabolism<sup><xref ref-type="bibr" rid="bib22">22</xref></sup> and Parfitt’s system.<sup><xref ref-type="bibr" rid="bib23">23</xref></sup> The formulas and correspondence between these 2D and 3D parameters were described in <xref rid="tbl2" ref-type="table">Table 2</xref>. All parameters assumed a plate model for the trabecular bone in the derivation of the equations used for calculation, as a previous study observed for the bone samples used in this study.<sup><xref ref-type="bibr" rid="bib17">17</xref></sup></p></sec><sec><title>Statistical analysis</title><p>Results were summarized by descriptive statistics as mean values with standard deviations and coefficient of variation. Wilcoxon signed-rank test and Spearman correlation test were adopted among all variables analysed in the study, after the normality test for the distribution of data by means of Shapiro–Wilks test. All the hypotheses testing were implemented in STATISTICA 8.0 (StatSoft, Inc., Tulsa, OK, USA) at a significance level of 0.05. The degree of agreement between the measured parameters from CBCT and histological data was compared using the method of Bland and Altman. In this method, the difference between the measurements was plotted against their mean, which was considered to be the best estimate of the true values.</p></sec></sec><sec><title>Results</title><p>In total, 36 alveolar bone samples (27 with implants and 9 without implants) were analysed. Normal distribution was checked first for all continuous variables according to Shapiro–Wilk test (<italic>P</italic><0.05). Descriptive statistics of all variables were presented in <xref rid="tbl3" ref-type="table">Table 3</xref>. Wilcoxon signed-rank test showed significant differences between the CBCT and histology for all morphometric parameters (<italic>P</italic><0.001). Although trabecular thickness (Tb.Th) and trabecular separation (Tb.Sp) were higher on CBCT images than on histological images, lower bone volume fraction (BV/TV) and trabecular number (Tb.N) were also found on CBCT images. The Spearman correlation between CBCT and histology for all analysed parameters showed significant correlation at <italic>P</italic><0.04.</p><p>Bland–Altman plots (<xref ref-type="fig" rid="fig2">Figure 2</xref>) indicated systematic bias, including constant bias for BV/TV, Tb.Sp and Tb.N, and proportional bias for Tb.Th. For the samples with implant, the smallest bias of measurements in Tb.Th (−0.12 mm) followed by Tb.Sp (−0.28 mm), Tb.N (+0.84 mm<sup>−1</sup>) and BV/TV (+23%). For the samples without implant, the smallest bias of measurements in Tb.Th (−0.13 mm) followed by Tb.Sp (−0.23 mm), Tb.N (+0.67 mm<sup>−1</sup>) and BV/TV (+14.02%). The lines of mean under the zero showed a slight overestimation of Tb.Sp and Tb.Th (<xref ref-type="fig" rid="fig2">Figure 2c and 2f</xref>), and the lines of mean above the zero demonstrated a slight underestimation of Tb.N by CBCT as compared with the histology (<xref ref-type="fig" rid="fig2">Figure 2g–2h</xref>).</p></sec><sec><title>Discussion</title><p>The present study showed that CBCT imager, with a spatial resolution as high as 80 μm, had significant correlations with histomorphometry on decalcified bone specimens for <italic>ex vivo</italic> quantification of peri-implant trabecular microstructure. In the evaluation of the agreement between CBCT and histology techniques, a combination of the Pearson’s correlation coefficient and Bland–Altman analyses was applied, which would help to avoid the potential affects by the observed outliers or extreme values.<sup><xref ref-type="bibr" rid="bib18">18</xref>,<xref ref-type="bibr" rid="bib24">24</xref></sup> In this study, we choose a ROI as far as 1mm away from the surface of the implant for both CBCT and histology techniques, due to the bone remodelling is greatest in the bone adjacent to the interface (within 1 mm of the implant) and decreases dramatically with increasing distance from the implant, according to a histomorphometric comparison in four species including humans.<sup><xref ref-type="bibr" rid="bib25">25</xref></sup> The reasons for choosing decalcified histological sectioning as the ‘gold standard’ were: (i) better resolution (to ∼6 μm) when compared with the CBCT imaging modality; (ii) the feasibility in colour detection for the bone segmentation; and (iii) no evidence at present that decalcification and embedding technique would significantly influence histomorphometric results.</p><p>In this study, comparisons between Tb.Th, Tb.Sp and Tb.N analyses showed highly significant correlation and good agreement between CBCT and histological images. This was well in accordance with a recent study which compared CBCT with micro-CT data on human jawbones.<sup><xref ref-type="bibr" rid="bib18">18</xref></sup> Interestingly, CBCT had a tendency to underestimate BV/TV in our study. The latter might be explained by differences between the voxel size (80 μm for CBCT <italic>vs.</italic> 6 μm for histology), resulting in smaller trabecular boundaries less well defined by CBCT than the histological images. This is consistent with studies which reported decreasing BV/TV and Tb.N with increasing pixel size (lower resolution).<sup><xref ref-type="bibr" rid="bib21 bib22 bib23 bib24 bib25 bib26">21–26</xref></sup> On the other hand, CBCT tended to overestimate Tb.Th and Tb.Sp, but the bias remained relatively low (−0.12 mm and −0.28 mm, respectively). This overestimation could be attributed to the sphere algorithm used for 3D measurement is influenced by the number of nodes (for Tb.Th) or shape and opening of the narrow cavities (for Tb.Sp), as observed in other comparisons of histomorphometry and micro-CT measurements.<sup><xref ref-type="bibr" rid="bib6">6</xref>,<xref ref-type="bibr" rid="bib24">24</xref></sup></p><p>However, caution should be taken when applying those trabecular parameters because systematic bias was also observed. There might be several reasons for the systematic biases between CBCT and histology. First, noise was present in the CBCT images as a close fine layer in the surface of titanium implants. Second, 3D CBCT results were calculated as an average value of different VOIs around the implant, while 2D histological results came from the most central section plane of the bone samples. Third, the histological sections in the study were ∼6 μm thick whereas the CBCT slice was 80 μm thick. Finally, the thresholding performed during image reconstruction and binarisation resulted in a systematic impact on subsequent quantitative results. A 10% change in the threshold of micro-CT causes a 5% change in BV/TV.<sup><xref ref-type="bibr" rid="bib27">27</xref></sup> Whether this linear relationship exists between morphometric parameters and the thresholding during the image processing remains to be examined for various CBCT imagers.</p><p>The quality of CT images could be largely influenced by metal artefacts, which in general leads to a combination of beam hardening, scattering, nonlinear partial volume effect and noise in CT images.<sup><xref ref-type="bibr" rid="bib28">28</xref></sup> According to micro-CT findings, a blurred border of 60 μm was found around 3.5 mm-diameter screw-shaped titanium implants.<sup><xref ref-type="bibr" rid="bib29">29</xref></sup> Although metal artefacts caused by titanium implant were present along the bone/implant direct interface in this study, specimen-specific threshold values were chosen manually based on the histogram of each image to minimize these artefacts. The intra-examiner reliability of CBCT measurements could be a further proof that the deviation derived from those manually adjustments is still desirable, suggested as another 3D bone structure analyses using CBCT.<sup><xref ref-type="bibr" rid="bib18">18</xref></sup> Moreover, it was shown that at the lower part of implant, the range and scale of the artefacts were significantly wider and larger than the upper and middle part.<sup><xref ref-type="bibr" rid="bib30">30</xref></sup> To compensate for the heterogeneity of artefact distribution around implants, morphometric analyses in our study were applied at three levels of VOIs along the bone/implant interface. In addition, there was little difference in correlations and biases between the groups with and without implants in this study, suggesting that CBCT is qualified for the evaluation of trabecular bone structures, regardless of the presence or absence of implants.</p><p>It has also to be acknowledged that even a micro-CT scanning with low resolution (e.g., large voxel size > 0.1 mm) relative to the size of the structure of interest may cause an underestimation of bone mineral density owing to partial-volume effects and overestimation of object thickness.<sup><xref ref-type="bibr" rid="bib22">22</xref></sup> On the other hand, it should also be considered that the fast development of CBCT techniques results in systems enabling to display bone details at a voxel size of 80 µm, being better than the thinnest trabecular thickness of mandibular bone, whether in dogs or humans.<sup><xref ref-type="bibr" rid="bib5">5</xref>,<xref ref-type="bibr" rid="bib31">31</xref></sup> From a clinical point of view, this may provides the possibility for jaw bone structural analysis bases on CBCT.</p><p>A limitation of the present study is that the bone samples were scanned <italic>ex vivo</italic> by CBCT. There was only one implant in each bone sample while CBCT scanning, which means the beam-hardening artefacts derived from multiple implants in the ROI (i.e., number of implants and corresponding spatial distribution) are not considered. Additionally, the stationary situation of the samples might have enhanced the visibility of the trabecular structures because the scans did not subject to patient’s movement. It could also be argued that there was no enough soft tissue surrounding the bone to mimic the real oral scanning situation. Despite this, a previous study already showed that CBCT yields similar morphometric parameters at the 3D level for all protocols with and without water as a mimic of soft-tissue while scanning.<sup><xref ref-type="bibr" rid="bib16">16</xref></sup></p><p>In summary, considering the good accuracy and strong correlations between CBCT-based and histological bone characteristics, it might be considered feasible to use a high resolution 3D CBCT for clinically diagnosing and analysing trabecular bone structure in general and more specifically around implants. Yet true clinical use can only follow after further studies focusing on the most accurate and reliable morphometric parameters, meanwhile identifying and dropping the biased ones. Such action may further enhance the diagnostic validity of CBCT-based analyses of peri-implant trabecular structures.</p></sec></body><back><ack><p>We are grateful to Jeanine Santermans and Marc Jans for their technical assistance. The study was supported by grants from the Interfaculty Council for Development Co-operation (IRO), KU Leuven, Belgium. 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(<bold>c</bold>) Histological slice of bone specimens (trichrome Masson stain; magnification, ×5) showed the trabecular bone (blue) and bone marrow (pink). (<bold>d</bold>) Trabecular bone in the binarized histological image at three manually selected ROIs. (<bold>e</bold>) Similar regions of interest were visually located in the 3D volume (80 μm resolution), corresponding to those in the 2D images (<bold>d</bold>) with a resolution of 6 μm.</p></caption><graphic xlink:href="boneres201410-f1"></graphic></fig><fig id="fig2"><label>Figure 2</label><caption><p>Bland–Altman plot comparing the agreement between cone-beam CT (CBCT) and histology in the bone samples with implant (<bold>a</bold>, <bold>c</bold>, <bold>e</bold>, <bold>g</bold>) and without implant (<bold>b</bold>, <bold>d</bold>, <bold>f</bold>, <bold>h</bold>) for the following bone structural parameters measurements: bone volume fraction (BV/TV), bone thickness (Tb.Th), bone separation (Tb.Sp) and trabecular number (Tb.N). Positive values represented larger BV/TV and Tb.N obtained from histological data compared with CBCT (<bold>a</bold>, <bold>b</bold>, <bold>g</bold>, <bold>h</bold>), while negative values showed smaller Tb.Th and Tb.Sp calculated from histology when comparing CBCT (<bold>c</bold>–<bold>f</bold>). The dotted lines on the Bland–Altman plot indicated the mean difference±1.96 standard deviations.</p></caption><graphic xlink:href="boneres201410-f2"></graphic></fig><table-wrap id="tbl1"><label>Table 1</label><caption><title>Distribution of alveolar bone samples in six experimental dogs</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col></colgroup><tbody valign="top"><tr><td align="left" valign="top" charoff="50">Group</td><td align="left" valign="top" charoff="50">I (R)</td><td align="left" valign="top" charoff="50">I (L)</td><td align="left" valign="top" charoff="50">P3 (R)</td><td align="left" valign="top" charoff="50">P3 (L)</td><td align="left" valign="top" charoff="50">P4 (R)</td><td align="left" valign="top" charoff="50">P4 (L)</td><td align="left" valign="top" charoff="50">Total</td></tr><tr><td align="left" valign="top" charoff="50">Bone with implants</td><td align="left" valign="top" charoff="50">4</td><td align="left" valign="top" charoff="50">5</td><td align="left" valign="top" charoff="50">5</td><td align="left" valign="top" charoff="50">5</td><td align="left" valign="top" charoff="50">4</td><td align="left" valign="top" charoff="50">4</td><td align="left" valign="top" charoff="50">27</td></tr><tr><td align="left" valign="top" charoff="50">Bone without implants</td><td align="left" valign="top" charoff="50">2</td><td align="left" valign="top" charoff="50">1</td><td align="left" valign="top" charoff="50">1</td><td align="left" valign="top" charoff="50">1</td><td align="left" valign="top" charoff="50">2</td><td align="left" valign="top" charoff="50">2</td><td align="left" valign="top" charoff="50">9</td></tr></tbody></table><table-wrap-foot><fn id="t1-tfoot1"><p>I, third maxillary incisors; P3, third mandibular premolars; P4, fourth mandibular premolars; R, right side; L, left side; implants, custom-made threaded, grade 5 pure titanium, machined surface, Ø=3.1 mm for I and 4.1 mm for P3 and P4, length=11 mm.</p></fn></table-wrap-foot></table-wrap><table-wrap id="tbl2"><label>Table 2</label><caption><title>Trabecular morphological parameters quantified from CBCT and histological images in selected regions of interest and volumes of interest, based on the parallel plate model</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col></colgroup><tbody valign="top"><tr><td align="left" valign="top" charoff="50">Morphological parameter</td><td align="left" valign="top" charoff="50">Abbreviation</td><td align="left" valign="top" charoff="50">Unit</td><td align="left" valign="top" charoff="50">2D measurements</td><td align="left" valign="top" charoff="50">3D measurements</td></tr><tr><td align="left" valign="top" charoff="50">Bone volume fraction</td><td align="left" valign="top" charoff="50">BV/TV</td><td align="left" valign="top" charoff="50">%</td><td align="left" valign="top" charoff="50">(A<sub>B</sub>/A<sub>T</sub>)100</td><td align="left" valign="top" charoff="50">BV/TV</td></tr><tr><td align="left" valign="top" charoff="50">Trabecular thickness</td><td align="left" valign="top" charoff="50">Tb.Th</td><td align="left" valign="top" charoff="50">mm</td><td align="left" valign="top" charoff="50">(2/1.199)(A<sub>B</sub>/P<sub>B</sub>)</td><td align="left" valign="top" charoff="50">2BV/BS</td></tr><tr><td align="left" valign="top" charoff="50">Trabecular separation</td><td align="left" valign="top" charoff="50">Tb.Sp</td><td align="left" valign="top" charoff="50">mm</td><td align="left" valign="top" charoff="50">(2/1.199)(A<sub>T</sub>−A<sub>B</sub>)/P<sub>B</sub></td><td align="left" valign="top" charoff="50">1/Tb.N–Tb.Th</td></tr><tr><td align="left" valign="top" charoff="50">Trabecular number</td><td align="left" valign="top" charoff="50">Tb.N</td><td align="left" valign="top" charoff="50">mm<sup>−1</sup></td><td align="left" valign="top" charoff="50">(1.199/2)(P<sub>B</sub>/A<sub>T</sub>)</td><td align="left" valign="top" charoff="50">(BV/TV)/Tb.Th</td></tr></tbody></table><table-wrap-foot><fn id="t2-tfoot1"><p>Abbreviations: A<sub>B</sub>, bone area; A<sub>T</sub>, total area; BS, bone surface; BV, bone volume; P<sub>B</sub>, bone perimeter; TV, tissue volume.</p></fn></table-wrap-foot></table-wrap><table-wrap id="tbl3"><label>Table 3</label><caption><title>Comparison of morphometric parameters obtained by CBCT and histology</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col></colgroup><thead valign="bottom"><tr><th rowspan="2" align="left" valign="top" charoff="50">Morphometric parameters</th><th colspan="2" align="center" valign="top" charoff="50">CBCT<hr></hr></th><th colspan="2" align="center" valign="top" charoff="50">Histology<hr></hr></th><th align="left" valign="top" charoff="50">Wilcoxon</th><th align="left" valign="top" charoff="50">Spearman’s</th></tr><tr><th align="left" valign="top" charoff="50">Mean±s.d.</th><th align="left" valign="top" charoff="50">CV</th><th align="left" valign="top" charoff="50">Mean±s.d.</th><th align="left" valign="top" charoff="50">CV</th><th align="left" valign="top" charoff="50"><italic>P</italic></th><th align="left" valign="top" charoff="50"><italic>r</italic> (<italic>P</italic>)</th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">Bone with implant (<italic>n</italic>=27)</td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td></tr><tr><td align="left" valign="top" charoff="50"> (BV/TV)/%</td><td align="left" valign="top" charoff="50">39.21±9.21</td><td align="left" valign="top" charoff="50">0.23</td><td align="left" valign="top" charoff="50">62.7±11.9</td><td align="left" valign="top" charoff="50">0.19</td><td align="left" valign="top" charoff="50"><0.001</td><td align="left" valign="top" charoff="50">0.65 (<0.001)</td></tr><tr><td align="left" valign="top" charoff="50"> Tb.Th/mm</td><td align="left" valign="top" charoff="50">0.43±0.05</td><td align="left" valign="top" charoff="50">0.11</td><td align="left" valign="top" charoff="50">0.31±0.02</td><td align="left" valign="top" charoff="50">0.07</td><td align="left" valign="top" charoff="50"><0.001</td><td align="left" valign="top" charoff="50">0.75 (<0.001)</td></tr><tr><td align="left" valign="top" charoff="50"> Tb.Sp/mm</td><td align="left" valign="top" charoff="50">0.57±0.13</td><td align="left" valign="top" charoff="50">0.22</td><td align="left" valign="top" charoff="50">0.29±0.10</td><td align="left" valign="top" charoff="50">0.35</td><td align="left" valign="top" charoff="50"><0.001</td><td align="left" valign="top" charoff="50">0.67 (<0.001)</td></tr><tr><td align="left" valign="top" charoff="50"> Tb.N/mm<sup>−1</sup></td><td align="left" valign="top" charoff="50">1.19±0.21</td><td align="left" valign="top" charoff="50">0.25</td><td align="left" valign="top" charoff="50">1.99±0.37</td><td align="left" valign="top" charoff="50">0.19</td><td align="left" valign="top" charoff="50"><0.001</td><td align="left" valign="top" charoff="50">0.85 (<0.001)</td></tr><tr><td align="left" valign="top" charoff="50">Bone without implant (<italic>n</italic>=9)</td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td></tr><tr><td align="left" valign="top" charoff="50"> (BV/TV)/%</td><td align="left" valign="top" charoff="50">36.26±6.15</td><td align="left" valign="top" charoff="50">0.33</td><td align="left" valign="top" charoff="50">50.50±7.72</td><td align="left" valign="top" charoff="50">0.16</td><td align="left" valign="top" charoff="50"><0.001</td><td align="left" valign="top" charoff="50">0.82 (<0.006)</td></tr><tr><td align="left" valign="top" charoff="50"> Tb.Th/mm</td><td align="left" valign="top" charoff="50">0.47±0.08</td><td align="left" valign="top" charoff="50">0.17</td><td align="left" valign="top" charoff="50">0.35±0.04</td><td align="left" valign="top" charoff="50">0.02</td><td align="left" valign="top" charoff="50"><0.001</td><td align="left" valign="top" charoff="50">0.68 (<0.04)</td></tr><tr><td align="left" valign="top" charoff="50"> Tb.Sp/mm</td><td align="left" valign="top" charoff="50">0.77±0.23</td><td align="left" valign="top" charoff="50">0.30</td><td align="left" valign="top" charoff="50">0.52±0.26</td><td align="left" valign="top" charoff="50">0.51</td><td align="left" valign="top" charoff="50"><0.001</td><td align="left" valign="top" charoff="50">0.88 (<0.002)</td></tr><tr><td align="left" valign="top" charoff="50"> Tb.N/mm<sup>−1</sup></td><td align="left" valign="top" charoff="50">0.73±0.13</td><td align="left" valign="top" charoff="50">0.19</td><td align="left" valign="top" charoff="50">1.38±0.29</td><td align="left" valign="top" charoff="50">0.21</td><td align="left" valign="top" charoff="50"><0.001</td><td align="left" valign="top" charoff="50">0.94 (<0.001)</td></tr></tbody></table><table-wrap-foot><fn id="t3-tfoot1"><p>Abbreviations: BV/TV, bone volume fraction; CBCT, cone-beam computed tomography; CV, 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