Association between Serum Matrix Metalloproteinase- (MMP-) 3 Levels and Systemic Lupus Erythematosus: A Meta-analysis
Identifieur interne : 000491 ( Pmc/Curation ); précédent : 000490; suivant : 000492Association between Serum Matrix Metalloproteinase- (MMP-) 3 Levels and Systemic Lupus Erythematosus: A Meta-analysis
Auteurs : Jiwon M. Lee [Corée du Sud] ; Andreas Kronbichler [Autriche] ; Se Jin Park [Corée du Sud] ; Seong Heon Kim [Corée du Sud] ; Kyoung Hee Han [Corée du Sud] ; Hee Gyung Kang [Corée du Sud] ; Il Soo Ha [Corée du Sud] ; Hae Il Cheong [Corée du Sud] ; Ki Hwan Kim [Corée du Sud] ; Gaeun Kim [Corée du Sud] ; Dong Soo Kim [Corée du Sud] ; Hyun Wook Chae [Corée du Sud] ; Chul Ho Lee [Corée du Sud] ; Keum Hwa Lee [Corée du Sud] ; Jae Il Shin [Corée du Sud]Source :
- Disease Markers [ 0278-0240 ] ; 2019.
Abstract
Matrix metalloproteinase (MMP) is an emerging disease marker in rheumatic diseases. This is a meta-analysis aimed at systematically reviewing association between serum MMP-3 levels and systematic lupus erythematosus (SLE) activity, which sought to raise interest in MMP-3 as a putative biomarker.
We conducted a meta-analysis of serum MMP-3 levels in patients with SLE and controls. We performed a PubMed search, EMBASE search, and forward search of the retrieved articles published until Oct. 1, 2018. In addition to this, we included data from a case-control study on a national pediatric SLE cohort, in which serum MMP-3 levels were measured in 11 SLE patients and 9 controls (unpublished). Subgroup analyses based on gender and disease activity were performed.
A total of 662 cases and 771 controls including 651 patients and 762 controls from 11 publications were studied. We observed significantly higher MMP-3 levels in SLE patients compared to healthy controls (
Our meta-analysis demonstrated significantly higher MMP-3 levels in SLE patients than in controls and in patients with renal involvement than in those without.
Url:
DOI: 10.1155/2019/9796735
PubMed: 31396295
PubMed Central: 6668546
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<author><name sortKey="Park, Se Jin" sort="Park, Se Jin" uniqKey="Park S" first="Se Jin" last="Park">Se Jin Park</name>
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<country xml:lang="fr">Corée du Sud</country>
<wicri:regionArea>Department of Pediatrics, Incheon St. Mary's Hospital, The Catholic University of Korea, Seoul</wicri:regionArea>
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<author><name sortKey="Kim, Gaeun" sort="Kim, Gaeun" uniqKey="Kim G" first="Gaeun" last="Kim">Gaeun Kim</name>
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<wicri:regionArea>Keimyung University College of Nursing, Daegu</wicri:regionArea>
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<author><name sortKey="Kim, Dong Soo" sort="Kim, Dong Soo" uniqKey="Kim D" first="Dong Soo" last="Kim">Dong Soo Kim</name>
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<country xml:lang="fr">Corée du Sud</country>
<wicri:regionArea>Department of Pediatrics, Yonsei University College of Medicine, Seoul</wicri:regionArea>
</affiliation>
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<author><name sortKey="Chae, Hyun Wook" sort="Chae, Hyun Wook" uniqKey="Chae H" first="Hyun Wook" last="Chae">Hyun Wook Chae</name>
<affiliation wicri:level="1"><nlm:aff id="I9">Department of Pediatrics, Yonsei University College of Medicine, Seoul, Republic of Korea</nlm:aff>
<country xml:lang="fr">Corée du Sud</country>
<wicri:regionArea>Department of Pediatrics, Yonsei University College of Medicine, Seoul</wicri:regionArea>
</affiliation>
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<author><name sortKey="Lee, Chul Ho" sort="Lee, Chul Ho" uniqKey="Lee C" first="Chul Ho" last="Lee">Chul Ho Lee</name>
<affiliation wicri:level="1"><nlm:aff id="I9">Department of Pediatrics, Yonsei University College of Medicine, Seoul, Republic of Korea</nlm:aff>
<country xml:lang="fr">Corée du Sud</country>
<wicri:regionArea>Department of Pediatrics, Yonsei University College of Medicine, Seoul</wicri:regionArea>
</affiliation>
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<author><name sortKey="Lee, Keum Hwa" sort="Lee, Keum Hwa" uniqKey="Lee K" first="Keum Hwa" last="Lee">Keum Hwa Lee</name>
<affiliation wicri:level="1"><nlm:aff id="I9">Department of Pediatrics, Yonsei University College of Medicine, Seoul, Republic of Korea</nlm:aff>
<country xml:lang="fr">Corée du Sud</country>
<wicri:regionArea>Department of Pediatrics, Yonsei University College of Medicine, Seoul</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Shin, Jae Il" sort="Shin, Jae Il" uniqKey="Shin J" first="Jae Il" last="Shin">Jae Il Shin</name>
<affiliation wicri:level="1"><nlm:aff id="I9">Department of Pediatrics, Yonsei University College of Medicine, Seoul, Republic of Korea</nlm:aff>
<country xml:lang="fr">Corée du Sud</country>
<wicri:regionArea>Department of Pediatrics, Yonsei University College of Medicine, Seoul</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="I10">Department of Pediatric Nephrology, Severance Children's Hospital, Seoul, Republic of Korea</nlm:aff>
<country xml:lang="fr">Corée du Sud</country>
<wicri:regionArea>Department of Pediatric Nephrology, Severance Children's Hospital, Seoul</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="I11">Institute of Kidney Disease Research, Yonsei University College of Medicine, Seoul, Republic of Korea</nlm:aff>
<country xml:lang="fr">Corée du Sud</country>
<wicri:regionArea>Institute of Kidney Disease Research, Yonsei University College of Medicine, Seoul</wicri:regionArea>
</affiliation>
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<series><title level="j">Disease Markers</title>
<idno type="ISSN">0278-0240</idno>
<idno type="eISSN">1875-8630</idno>
<imprint><date when="2019">2019</date>
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<front><div type="abstract" xml:lang="en"><sec><title>Introduction</title>
<p> Matrix metalloproteinase (MMP) is an emerging disease marker in rheumatic diseases. This is a meta-analysis aimed at systematically reviewing association between serum MMP-3 levels and systematic lupus erythematosus (SLE) activity, which sought to raise interest in MMP-3 as a putative biomarker. </p>
</sec>
<sec><title>Methods</title>
<p> We conducted a meta-analysis of serum MMP-3 levels in patients with SLE and controls. We performed a PubMed search, EMBASE search, and forward search of the retrieved articles published until Oct. 1, 2018. In addition to this, we included data from a case-control study on a national pediatric SLE cohort, in which serum MMP-3 levels were measured in 11 SLE patients and 9 controls (unpublished). Subgroup analyses based on gender and disease activity were performed. </p>
</sec>
<sec><title>Results</title>
<p> A total of 662 cases and 771 controls including 651 patients and 762 controls from 11 publications were studied. We observed significantly higher MMP-3 levels in SLE patients compared to healthy controls (<italic>P</italic>
< 0.001, Hedges' <italic>g</italic>
: 2.104, 95% CI 1.426-2.782). In subgroup analyses, we found a significant elevation of MMP-3 in the patients with nephritis compared to those without (<italic>P</italic>
= 0.006, Hedges' <italic>g</italic>
: 0.611, 95% CI 0.611-1.704). This finding was consistent between patients with persistent proteinuria and those without (<italic>P</italic>
= 0.023, Hedges' <italic>g</italic>
: 1.535, 95% CI 0.207-2.862). Meta-analysis showed no association between MMP-3 levels and gender or anti-double strand DNA antibody titer. </p>
</sec>
<sec><title>Conclusions</title>
<p> Our meta-analysis demonstrated significantly higher MMP-3 levels in SLE patients than in controls and in patients with renal involvement than in those without.</p>
</sec>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Dis Markers</journal-id>
<journal-id journal-id-type="iso-abbrev">Dis. Markers</journal-id>
<journal-id journal-id-type="publisher-id">DM</journal-id>
<journal-title-group><journal-title>Disease Markers</journal-title>
</journal-title-group>
<issn pub-type="ppub">0278-0240</issn>
<issn pub-type="epub">1875-8630</issn>
<publisher><publisher-name>Hindawi</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31396295</article-id>
<article-id pub-id-type="pmc">6668546</article-id>
<article-id pub-id-type="doi">10.1155/2019/9796735</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Association between Serum Matrix Metalloproteinase- (MMP-) 3 Levels and Systemic Lupus Erythematosus: A Meta-analysis</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-3932-614X</contrib-id>
<name><surname>Lee</surname>
<given-names>Jiwon M.</given-names>
</name>
<xref ref-type="aff" rid="I1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-2945-2946</contrib-id>
<name><surname>Kronbichler</surname>
<given-names>Andreas</given-names>
</name>
<xref ref-type="aff" rid="I2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Park</surname>
<given-names>Se Jin</given-names>
</name>
<xref ref-type="aff" rid="I3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-8003-3010</contrib-id>
<name><surname>Kim</surname>
<given-names>Seong Heon</given-names>
</name>
<xref ref-type="aff" rid="I4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-6830-7311</contrib-id>
<name><surname>Han</surname>
<given-names>Kyoung Hee</given-names>
</name>
<xref ref-type="aff" rid="I5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-8323-5320</contrib-id>
<name><surname>Kang</surname>
<given-names>Hee Gyung</given-names>
</name>
<xref ref-type="aff" rid="I6"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ha</surname>
<given-names>Il Soo</given-names>
</name>
<xref ref-type="aff" rid="I6"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-7556-1265</contrib-id>
<name><surname>Cheong</surname>
<given-names>Hae Il</given-names>
</name>
<xref ref-type="aff" rid="I6"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kim</surname>
<given-names>Ki Hwan</given-names>
</name>
<xref ref-type="aff" rid="I7"><sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kim</surname>
<given-names>Gaeun</given-names>
</name>
<xref ref-type="aff" rid="I8"><sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kim</surname>
<given-names>Dong Soo</given-names>
</name>
<xref ref-type="aff" rid="I9"><sup>9</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chae</surname>
<given-names>Hyun Wook</given-names>
</name>
<xref ref-type="aff" rid="I9"><sup>9</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lee</surname>
<given-names>Chul Ho</given-names>
</name>
<xref ref-type="aff" rid="I9"><sup>9</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lee</surname>
<given-names>Keum Hwa</given-names>
</name>
<xref ref-type="aff" rid="I9"><sup>9</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-2326-1820</contrib-id>
<name><surname>Shin</surname>
<given-names>Jae Il</given-names>
</name>
<email>shinji@yuhs.ac</email>
<xref ref-type="aff" rid="I9"><sup>9</sup>
</xref>
<xref ref-type="aff" rid="I10"><sup>10</sup>
</xref>
<xref ref-type="aff" rid="I11"><sup>11</sup>
</xref>
</contrib>
</contrib-group>
<aff id="I1"><sup>1</sup>
Department of Pediatrics, Chungnam National University Hospital, Daejeon, Republic of Korea</aff>
<aff id="I2"><sup>2</sup>
Department of Internal Medicine IV (Nephrology and Hypertension), Medical University Innsbruck, Innsbruck, Austria</aff>
<aff id="I3"><sup>3</sup>
Department of Pediatrics, Ajou University Hospital, Ajou University School of Medicine, Suwon, Republic of Korea</aff>
<aff id="I4"><sup>4</sup>
Department of Pediatrics, Pusan National University Children's Hospital, Yangsan, Republic of Korea</aff>
<aff id="I5"><sup>5</sup>
Department of Pediatrics, Jeju National University School of Medicine, Jeju, Republic of Korea</aff>
<aff id="I6"><sup>6</sup>
Department of Pediatrics, Seoul National University Children's Hospital, Seoul, Republic of Korea</aff>
<aff id="I7"><sup>7</sup>
Department of Pediatrics, Incheon St. Mary's Hospital, The Catholic University of Korea, Seoul, Republic of Korea</aff>
<aff id="I8"><sup>8</sup>
Keimyung University College of Nursing, Daegu, Republic of Korea</aff>
<aff id="I9"><sup>9</sup>
Department of Pediatrics, Yonsei University College of Medicine, Seoul, Republic of Korea</aff>
<aff id="I10"><sup>10</sup>
Department of Pediatric Nephrology, Severance Children's Hospital, Seoul, Republic of Korea</aff>
<aff id="I11"><sup>11</sup>
Institute of Kidney Disease Research, Yonsei University College of Medicine, Seoul, Republic of Korea</aff>
<author-notes><fn fn-type="other"><p>Academic Editor: Massimiliano Castellazzi</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>18</day>
<month>7</month>
<year>2019</year>
</pub-date>
<volume>2019</volume>
<elocation-id>9796735</elocation-id>
<history><date date-type="received"><day>5</day>
<month>2</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>4</day>
<month>6</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2019 Jiwon M. Lee et al.</copyright-statement>
<copyright-year>2019</copyright-year>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract><sec><title>Introduction</title>
<p> Matrix metalloproteinase (MMP) is an emerging disease marker in rheumatic diseases. This is a meta-analysis aimed at systematically reviewing association between serum MMP-3 levels and systematic lupus erythematosus (SLE) activity, which sought to raise interest in MMP-3 as a putative biomarker. </p>
</sec>
<sec><title>Methods</title>
<p> We conducted a meta-analysis of serum MMP-3 levels in patients with SLE and controls. We performed a PubMed search, EMBASE search, and forward search of the retrieved articles published until Oct. 1, 2018. In addition to this, we included data from a case-control study on a national pediatric SLE cohort, in which serum MMP-3 levels were measured in 11 SLE patients and 9 controls (unpublished). Subgroup analyses based on gender and disease activity were performed. </p>
</sec>
<sec><title>Results</title>
<p> A total of 662 cases and 771 controls including 651 patients and 762 controls from 11 publications were studied. We observed significantly higher MMP-3 levels in SLE patients compared to healthy controls (<italic>P</italic>
< 0.001, Hedges' <italic>g</italic>
: 2.104, 95% CI 1.426-2.782). In subgroup analyses, we found a significant elevation of MMP-3 in the patients with nephritis compared to those without (<italic>P</italic>
= 0.006, Hedges' <italic>g</italic>
: 0.611, 95% CI 0.611-1.704). This finding was consistent between patients with persistent proteinuria and those without (<italic>P</italic>
= 0.023, Hedges' <italic>g</italic>
: 1.535, 95% CI 0.207-2.862). Meta-analysis showed no association between MMP-3 levels and gender or anti-double strand DNA antibody titer. </p>
</sec>
<sec><title>Conclusions</title>
<p> Our meta-analysis demonstrated significantly higher MMP-3 levels in SLE patients than in controls and in patients with renal involvement than in those without.</p>
</sec>
</abstract>
<funding-group><award-group><funding-source>Chungnam National University Hospital</funding-source>
</award-group>
</funding-group>
</article-meta>
</front>
<floats-group><fig id="fig1" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Flow diagram of search strategy.</p>
</caption>
<graphic xlink:href="DM2019-9796735.001"></graphic>
</fig>
<fig id="fig2" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>Forest plot of random effects meta-analysis of MMP-3 levels in SLE patients compared with healthy controls.</p>
</caption>
<graphic xlink:href="DM2019-9796735.002"></graphic>
</fig>
<fig id="fig3" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>Forest plot of random effects meta-analysis of MMP-3 levels in SLE patients compared with healthy controls (excluding pediatric data from KPS).</p>
</caption>
<graphic xlink:href="DM2019-9796735.003"></graphic>
</fig>
<fig id="fig4" orientation="portrait" position="float"><label>Figure 4</label>
<caption><p>Forest plot of random effects meta-analysis of MMP-3 levels in SLE patients; male vs. female.</p>
</caption>
<graphic xlink:href="DM2019-9796735.004"></graphic>
</fig>
<fig id="fig5" orientation="portrait" position="float"><label>Figure 5</label>
<caption><p>Forest plot of random effects meta-analysis of MMP-3 levels in SLE patients; with vs. without nephritis.</p>
</caption>
<graphic xlink:href="DM2019-9796735.005"></graphic>
</fig>
<fig id="fig6" orientation="portrait" position="float"><label>Figure 6</label>
<caption><p>Forest plot of random effects meta-analysis of MMP-3 levels in SLE patients; with vs. without proteinuria.</p>
</caption>
<graphic xlink:href="DM2019-9796735.006"></graphic>
</fig>
<fig id="fig7" orientation="portrait" position="float"><label>Figure 7</label>
<caption><p>Forest plot of random effects meta-analysis of MMP-3 levels in SLE patients; with vs. without increased anti-dsDNA titer.</p>
</caption>
<graphic xlink:href="DM2019-9796735.007"></graphic>
</fig>
<fig id="fig8" orientation="portrait" position="float"><label>Figure 8</label>
<caption><p>Funnel plot of standard error in meta-analysis of MMP-3 levels in SLE patients compared with healthy controls.</p>
</caption>
<graphic xlink:href="DM2019-9796735.008"></graphic>
</fig>
<table-wrap id="tab1" content-type="sidewaystable" orientation="portrait" position="float"><label>Table 1</label>
<caption><p>Characteristics of all studies included in the meta-analysis.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="2" colspan="1">Author (year)</th>
<th align="center" rowspan="2" colspan="1">Study groups</th>
<th align="center" rowspan="2" colspan="1"><italic>N</italic>
</th>
<th align="center" rowspan="1" colspan="1">Sex</th>
<th align="center" rowspan="1" colspan="1">Age</th>
<th align="center" rowspan="2" colspan="1">Subgroup analysis within SLE</th>
<th align="center" rowspan="1" colspan="1">MMP-3 in SLE</th>
<th align="center" rowspan="1" colspan="1">MMP-3 in HC</th>
<th align="center" rowspan="2" colspan="1">ELISA kit used</th>
</tr>
<tr><th align="center" rowspan="1" colspan="1">M/F</th>
<th align="center" rowspan="1" colspan="1">Mean (SD or range)</th>
<th align="center" rowspan="1" colspan="1">Mean (SD or range)</th>
<th align="center" rowspan="1" colspan="1">Mean (SD or range)</th>
</tr>
</thead>
<tbody><tr><td align="left" rowspan="2" colspan="1">Jin et al. (2013) [<xref rid="B15" ref-type="bibr">15</xref>
]</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">31</td>
<td align="center" rowspan="1" colspan="1">0/31</td>
<td align="center" rowspan="1" colspan="1">48.7 (12.7)</td>
<td align="center" rowspan="2" colspan="1">—</td>
<td align="center" rowspan="2" colspan="1">25.2 (23.4)</td>
<td align="center" rowspan="2" colspan="1">10.2 (4.4)</td>
<td align="center" rowspan="2" colspan="1">Quantikine; R&D Systems Inc., UK</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">150</td>
<td align="center" rowspan="1" colspan="1">0/150</td>
<td align="center" rowspan="1" colspan="1">45.8 (11.3)</td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="2" colspan="1">Zhu et al. (2015)</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">60</td>
<td align="center" rowspan="1" colspan="1">3/57</td>
<td align="center" rowspan="1" colspan="1">33.3 (10.8)</td>
<td align="center" rowspan="2" colspan="1">—</td>
<td align="center" rowspan="2" colspan="1">21.4 (7.3)</td>
<td align="center" rowspan="2" colspan="1">14.4 (8.4)</td>
<td align="center" rowspan="2" colspan="1">Quantikine; R&D Systems Inc., UK</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">60</td>
<td align="center" rowspan="1" colspan="1">3/57</td>
<td align="center" rowspan="1" colspan="1">33.4 (10.9)</td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="2" colspan="1">De Leeuw et al. (2006) [<xref rid="B16" ref-type="bibr">16</xref>
]</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">72</td>
<td align="center" rowspan="1" colspan="1">9/63</td>
<td align="center" rowspan="1" colspan="1">41.0 (12.0)</td>
<td align="center" rowspan="2" colspan="1">—</td>
<td align="center" rowspan="2" colspan="1">19 (14.1)</td>
<td align="center" rowspan="2" colspan="1">8.0 (4.4)</td>
<td align="center" rowspan="2" colspan="1">BioSource, Europe S.A., Belgium</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">36</td>
<td align="center" rowspan="1" colspan="1">3/33</td>
<td align="center" rowspan="1" colspan="1">41.0 (12.0)</td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="3" colspan="1">Ribbens et al. (2002) [<xref rid="B17" ref-type="bibr">17</xref>
]</td>
<td align="center" rowspan="1" colspan="1">Cutaneous lupus</td>
<td align="center" rowspan="1" colspan="1">7</td>
<td align="center" rowspan="1" colspan="1">0/7</td>
<td align="center" rowspan="1" colspan="1">34 (15-57)</td>
<td align="center" rowspan="1" colspan="1">Cutaneous lupus</td>
<td align="center" rowspan="3" colspan="1">11.5 (4.4) (female data)</td>
<td align="center" rowspan="3" colspan="1">9.2 (2.8)</td>
<td align="center" rowspan="3" colspan="1">BioSource, Europe S.A., Belgium</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">Renal lupus</td>
<td align="center" rowspan="1" colspan="1">7</td>
<td align="center" rowspan="1" colspan="1">2/5</td>
<td align="center" rowspan="1" colspan="1">30 (15-54)</td>
<td align="center" rowspan="1" colspan="1">Renal lupus</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">96</td>
<td align="center" rowspan="1" colspan="1">50/46</td>
<td align="center" rowspan="1" colspan="1">44 (25-64)</td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="2" colspan="1">Zucker et al. (1999) [<xref rid="B12" ref-type="bibr">12</xref>
]</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">73</td>
<td align="center" rowspan="1" colspan="1">N/A</td>
<td align="center" rowspan="1" colspan="1">N/A</td>
<td align="center" rowspan="2" colspan="1">—</td>
<td align="center" rowspan="2" colspan="1">416.0 (252.0)</td>
<td align="center" rowspan="2" colspan="1">125.0 (93.0)</td>
<td align="center" rowspan="2" colspan="1">In-house method using human Ab (Mac078, Celltech)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">39</td>
<td align="center" rowspan="1" colspan="1">N/A</td>
<td align="center" rowspan="1" colspan="1">N/A</td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="2" colspan="1">Ichikawa et al. (1998) [<xref rid="B18" ref-type="bibr">18</xref>
]</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">21</td>
<td align="center" rowspan="1" colspan="1">3/18</td>
<td align="center" rowspan="1" colspan="1">38.2 (13.5)</td>
<td align="center" rowspan="2" colspan="1">—</td>
<td align="center" rowspan="2" colspan="1">239.1 (199.6)</td>
<td align="center" rowspan="2" colspan="1">63 (64.1)</td>
<td align="center" rowspan="2" colspan="1">Fuji Chemical Industries Ltd., Toyama, Japan</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">20</td>
<td align="center" rowspan="1" colspan="1">0/20</td>
<td align="center" rowspan="1" colspan="1">56.8 (4.6)</td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="2" colspan="1">Kotajima et al. (1998)</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">124</td>
<td align="center" rowspan="1" colspan="1">8/116</td>
<td align="center" rowspan="1" colspan="1">N/A</td>
<td align="center" rowspan="2" colspan="1">With or without dsDNA</td>
<td align="center" rowspan="2" colspan="1">193.0 (171.5)</td>
<td align="center" rowspan="2" colspan="1">61.8 (33.9)</td>
<td align="center" rowspan="2" colspan="1">In-house method using human Ab (NB1RGB)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">117</td>
<td align="center" rowspan="1" colspan="1">67/50</td>
<td align="center" rowspan="1" colspan="1">N/A</td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="2" colspan="1">Akiyama et al. (1997) [<xref rid="B19" ref-type="bibr">19</xref>
]</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">13</td>
<td align="center" rowspan="1" colspan="1">5/7</td>
<td align="center" rowspan="1" colspan="1">35.6 (3.5)</td>
<td align="center" rowspan="2" colspan="1">—</td>
<td align="center" rowspan="2" colspan="1">155.7 (23.4)</td>
<td align="center" rowspan="2" colspan="1">61.7 (3.15)</td>
<td align="center" rowspan="2" colspan="1">Fuji Chemical Industries Ltd., Toyama, Japan</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">154</td>
<td align="center" rowspan="1" colspan="1">N/A</td>
<td align="center" rowspan="1" colspan="1">N/A</td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="2" colspan="1">Shingu et al. (1995) [<xref rid="B20" ref-type="bibr">20</xref>
]</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">67</td>
<td align="center" rowspan="1" colspan="1">6/61</td>
<td align="center" rowspan="1" colspan="1">46.5 (15.6)</td>
<td align="center" rowspan="2" colspan="1">—</td>
<td align="center" rowspan="2" colspan="1">117.3 (107.4)</td>
<td align="center" rowspan="2" colspan="1">42.1 (29.2)</td>
<td align="center" rowspan="2" colspan="1">Fuji Chemical Industries Ltd., Toyama, Japan</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">170</td>
<td align="center" rowspan="1" colspan="1">50/120</td>
<td align="center" rowspan="1" colspan="1">N/A</td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="2" colspan="1">Zucker et al. (1994) [<xref rid="B21" ref-type="bibr">21</xref>
]</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">17</td>
<td align="center" rowspan="1" colspan="1">3/14</td>
<td align="center" rowspan="1" colspan="1">36.2 (N/A)</td>
<td align="center" rowspan="2" colspan="1">—</td>
<td align="center" rowspan="2" colspan="1">258.4 (124.3)</td>
<td align="center" rowspan="2" colspan="1">50.0 (124.3)</td>
<td align="center" rowspan="2" colspan="1">In-house method using human Ab (Mac078, Celltech)</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">53</td>
<td align="center" rowspan="1" colspan="1">30/23</td>
<td align="center" rowspan="1" colspan="1">42.0 (N/A)</td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="2" colspan="1">Gheita et al. (2015) [<xref rid="B22" ref-type="bibr">22</xref>
]</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">42</td>
<td align="center" rowspan="1" colspan="1">0/42</td>
<td align="center" rowspan="1" colspan="1">33.2 (11.6)</td>
<td align="center" rowspan="2" colspan="1">With or without nephritis</td>
<td align="center" rowspan="2" colspan="1">80.9 (45.8)</td>
<td align="center" rowspan="2" colspan="1">10.01 (2.6)</td>
<td align="center" rowspan="2" colspan="1">N/A</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">30</td>
<td align="center" rowspan="1" colspan="1">0/30</td>
<td align="center" rowspan="1" colspan="1">N/A</td>
</tr>
<tr><td align="center" colspan="9" rowspan="1"><hr></hr>
</td>
</tr>
<tr><td align="left" rowspan="2" colspan="1">KPS study (unpublished)</td>
<td align="center" rowspan="1" colspan="1">SLE</td>
<td align="center" rowspan="1" colspan="1">11</td>
<td align="center" rowspan="1" colspan="1">3/8</td>
<td align="center" rowspan="1" colspan="1">14.5 (11.8-18)</td>
<td align="center" rowspan="1" colspan="1">With vs. without nephritis</td>
<td align="center" rowspan="2" colspan="1">195.3 (50.3)</td>
<td align="center" rowspan="2" colspan="1">26.4 (19.3)</td>
<td align="center" rowspan="2" colspan="1">Ab Frontier, Seoul, Korea</td>
</tr>
<tr><td align="center" rowspan="1" colspan="1">HC</td>
<td align="center" rowspan="1" colspan="1">9</td>
<td align="center" rowspan="1" colspan="1">2/7</td>
<td align="center" rowspan="1" colspan="1">12.2 (10.0-15.0)</td>
<td align="center" rowspan="1" colspan="1">With vs. without dsDNA</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>Abbreviations used: dsDNA: double-stranded DNA antibodies; F: female; HC: healthy controls; M: male; MMP-3: matrix metalloproteinase-3; <italic>N</italic>
: number; N/A: not available; SD: standard deviation; SLE: systemic lupus erythematosus. MMP-3 levels were all measured in ng/mL.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="tab2" content-type="sidewaystable" orientation="portrait" position="float"><label>Table 2</label>
<caption><p>Summary of the results of meta-analysis.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="2" colspan="1">Group-wise</th>
<th align="center" rowspan="2" colspan="1">No. of studies</th>
<th align="center" colspan="2" rowspan="2">No. of subjects</th>
<th align="center" colspan="4" rowspan="1">Meta-analysis</th>
<th align="center" colspan="3" rowspan="1">Heterogeneity</th>
<th align="center" rowspan="1" colspan="1">Egger's bias</th>
</tr>
<tr><th align="center" rowspan="1" colspan="1">Hedges' <italic>g</italic>
</th>
<th align="center" colspan="2" rowspan="1">95% CI</th>
<th align="center" rowspan="1" colspan="1"><italic>P</italic>
value</th>
<th align="center" rowspan="1" colspan="1"><italic>I</italic>
<sup>2</sup>
(%)</th>
<th align="center" rowspan="1" colspan="1">Tau<sup>2</sup>
</th>
<th align="center" rowspan="1" colspan="1"><italic>P</italic>
value</th>
<th align="center" rowspan="1" colspan="1"><italic>P</italic>
value</th>
</tr>
</thead>
<tbody><tr><td align="left" rowspan="1" colspan="1"><italic>Total</italic>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">SLE vs. HC (including KPS data)</td>
<td align="center" rowspan="1" colspan="1">12</td>
<td align="center" rowspan="1" colspan="1">SLE 662</td>
<td align="center" rowspan="1" colspan="1">HC 771</td>
<td align="center" rowspan="1" colspan="1">2.104</td>
<td align="center" rowspan="1" colspan="1">1.426</td>
<td align="center" rowspan="1" colspan="1">2.782</td>
<td align="center" rowspan="1" colspan="1"><0.001</td>
<td align="center" rowspan="1" colspan="1">96.046</td>
<td align="center" rowspan="1" colspan="1">1.308</td>
<td align="center" rowspan="1" colspan="1"><0.001</td>
<td align="center" rowspan="1" colspan="1">0.02</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">SLE vs. HC (excluding KPS data)</td>
<td align="center" rowspan="1" colspan="1">11</td>
<td align="center" rowspan="1" colspan="1">SLE 651</td>
<td align="center" rowspan="1" colspan="1">HC 762</td>
<td align="center" rowspan="1" colspan="1">1.963</td>
<td align="center" rowspan="1" colspan="1">1.276</td>
<td align="center" rowspan="1" colspan="1">2.650</td>
<td align="center" rowspan="1" colspan="1"><0.001</td>
<td align="center" rowspan="1" colspan="1">96.217</td>
<td align="center" rowspan="1" colspan="1">1.256</td>
<td align="center" rowspan="1" colspan="1"><0.001</td>
<td align="center" rowspan="1" colspan="1">0.02</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>Sex</italic>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">Male vs. female SLE</td>
<td align="center" rowspan="1" colspan="1">2</td>
<td align="center" rowspan="1" colspan="1">Male 6</td>
<td align="center" rowspan="1" colspan="1">Female 26</td>
<td align="center" rowspan="1" colspan="1">0.360</td>
<td align="center" rowspan="1" colspan="1">-0.491</td>
<td align="center" rowspan="1" colspan="1">1.212</td>
<td align="center" rowspan="1" colspan="1">0.407</td>
<td align="center" rowspan="1" colspan="1">0.000</td>
<td align="center" rowspan="1" colspan="1">0.000</td>
<td align="center" rowspan="1" colspan="1">0.369</td>
<td align="center" rowspan="1" colspan="1">—</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>Renal manifestation</italic>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">SLE with vs. without nephritis</td>
<td align="center" rowspan="1" colspan="1">3</td>
<td align="center" rowspan="1" colspan="1">With 53</td>
<td align="center" rowspan="1" colspan="1">Without 39</td>
<td align="center" rowspan="1" colspan="1">0.639</td>
<td align="center" rowspan="1" colspan="1">0.221</td>
<td align="center" rowspan="1" colspan="1">1.057</td>
<td align="center" rowspan="1" colspan="1">0.003</td>
<td align="center" rowspan="1" colspan="1">0.000</td>
<td align="center" rowspan="1" colspan="1">0.000</td>
<td align="center" rowspan="1" colspan="1">0.841</td>
<td align="center" rowspan="1" colspan="1">—</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">SLE with vs. without proteinuria</td>
<td align="center" rowspan="1" colspan="1">2</td>
<td align="center" rowspan="1" colspan="1">With 57</td>
<td align="center" rowspan="1" colspan="1">Without 82</td>
<td align="center" rowspan="1" colspan="1">1.535</td>
<td align="center" rowspan="1" colspan="1">0.207</td>
<td align="center" rowspan="1" colspan="1">2.862</td>
<td align="center" rowspan="1" colspan="1">0.023</td>
<td align="center" rowspan="1" colspan="1">79.694</td>
<td align="center" rowspan="1" colspan="1">0.751</td>
<td align="center" rowspan="1" colspan="1">0.023</td>
<td align="center" rowspan="1" colspan="1">—</td>
</tr>
<tr><td align="left" rowspan="1" colspan="1"><italic>Disease activity</italic>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td align="left" rowspan="1" colspan="1">SLE (+) vs. (-) anti-dsDNA</td>
<td align="center" rowspan="1" colspan="1">2</td>
<td align="center" rowspan="1" colspan="1">(+) 57</td>
<td align="center" rowspan="1" colspan="1">(-) 82</td>
<td align="center" rowspan="1" colspan="1">0.094</td>
<td align="center" rowspan="1" colspan="1">-1.352</td>
<td align="center" rowspan="1" colspan="1">1.540</td>
<td align="center" rowspan="1" colspan="1">0.898</td>
<td align="center" rowspan="1" colspan="1">83.360</td>
<td align="center" rowspan="1" colspan="1">0.924</td>
<td align="center" rowspan="1" colspan="1">0.014</td>
<td align="center" rowspan="1" colspan="1">—</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>Abbreviations used: dsDNA: double-stranded DNA antibodies; HC: healthy controls; SLE: systemic lupus erythematosus. <italic>P</italic>
values were all two-tailed.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
</record>
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