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Validating cone-beam computed tomography for peri-implant bone morphometric analysis

Identifieur interne : 005E49 ( Ncbi/Merge ); précédent : 005E48; suivant : 005E50

Validating cone-beam computed tomography for peri-implant bone morphometric analysis

Auteurs : Yan Huang [Belgique, République populaire de Chine] ; Jeroen Van Dessel [Belgique] ; Maarten Depypere [Belgique] ; Mostafa Ezeldeen [Belgique] ; Alexandru Andrei Iliescu [Roumanie] ; Emanuela Dos Santos [Brésil] ; Ivo Lambrichts [Belgique] ; Xin Liang [République populaire de Chine] ; Reinhilde Jacobs [Belgique]

Source :

RBID : PMC:4472132

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 n=27 vs. without implants n=9) from six mongrel dogs, were scanned ex vivo 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 (P<0.001). Both measurements on the peri-implant trabecular bone structure showed moderate to high correlation (r=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.


Url:
DOI: 10.1038/boneres.2014.10
PubMed: 26273522
PubMed Central: 4472132

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PMC:4472132

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<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>
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<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>
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<label>*</label>
<email>reinhilde.jacobs@med.kuleuven.be</email>
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</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>
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<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>
<floats-group>
<fig id="fig1">
<label>Figure 1</label>
<caption>
<p>(
<bold>a</bold>
) Three-dimensional models reconstructed from cone-beam computed tomography images in the coronal plane (mesial–distal view). (
<bold>b</bold>
) Three VOIs (coronal, middle and apical levels) were automatically selected from (
<bold>a</bold>
) along the surface of implant by a custom processing algorithm based on thresholding segmentation. (
<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, coefficient of variation; s.d., standard deviation; Tb.N, trabecular number; Tb.Sp, trabecular separation; Tb.Th, trabecular thickness.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
<affiliations>
<list>
<country>
<li>Belgique</li>
<li>Brésil</li>
<li>Roumanie</li>
<li>République populaire de Chine</li>
</country>
</list>
<tree>
<country name="Belgique">
<noRegion>
<name sortKey="Huang, Yan" sort="Huang, Yan" uniqKey="Huang Y" first="Yan" last="Huang">Yan Huang</name>
</noRegion>
<name sortKey="Depypere, Maarten" sort="Depypere, Maarten" uniqKey="Depypere M" first="Maarten" last="Depypere">Maarten Depypere</name>
<name sortKey="Dessel, Jeroen Van" sort="Dessel, Jeroen Van" uniqKey="Dessel J" first="Jeroen Van" last="Dessel">Jeroen Van Dessel</name>
<name sortKey="Ezeldeen, Mostafa" sort="Ezeldeen, Mostafa" uniqKey="Ezeldeen M" first="Mostafa" last="Ezeldeen">Mostafa Ezeldeen</name>
<name sortKey="Jacobs, Reinhilde" sort="Jacobs, Reinhilde" uniqKey="Jacobs R" first="Reinhilde" last="Jacobs">Reinhilde Jacobs</name>
<name sortKey="Lambrichts, Ivo" sort="Lambrichts, Ivo" uniqKey="Lambrichts I" first="Ivo" last="Lambrichts">Ivo Lambrichts</name>
</country>
<country name="République populaire de Chine">
<noRegion>
<name sortKey="Huang, Yan" sort="Huang, Yan" uniqKey="Huang Y" first="Yan" last="Huang">Yan Huang</name>
</noRegion>
<name sortKey="Liang, Xin" sort="Liang, Xin" uniqKey="Liang X" first="Xin" last="Liang">Xin Liang</name>
</country>
<country name="Roumanie">
<noRegion>
<name sortKey="Iliescu, Alexandru Andrei" sort="Iliescu, Alexandru Andrei" uniqKey="Iliescu A" first="Alexandru Andrei" last="Iliescu">Alexandru Andrei Iliescu</name>
</noRegion>
</country>
<country name="Brésil">
<noRegion>
<name sortKey="Santos, Emanuela Dos" sort="Santos, Emanuela Dos" uniqKey="Santos E" first="Emanuela Dos" last="Santos">Emanuela Dos Santos</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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