Association between Serum Matrix Metalloproteinase- (MMP-) 3 Levels and Systemic Lupus Erythematosus: A Meta-analysis
Identifieur interne : 000898 ( Ncbi/Merge ); précédent : 000897; suivant : 000899Association 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study on a national pediatric SLE cohort, in which serum MMP-3 levels were measured in 11 SLE patients and 9 controls (unpublished).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.
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DOI: 10.1155/2019/9796735
PubMed: 31396295
PubMed Central: 6668546
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Lee</name><affiliation wicri:level="1"><nlm:aff id="I1">Department of Pediatrics, Chungnam National University Hospital, Daejeon, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Pediatrics, Chungnam National University Hospital, Daejeon</wicri:regionArea><wicri:noRegion>Daejeon</wicri:noRegion></affiliation></author><author><name sortKey="Kronbichler, Andreas" sort="Kronbichler, Andreas" uniqKey="Kronbichler A" first="Andreas" last="Kronbichler">Andreas Kronbichler</name><affiliation wicri:level="1"><nlm:aff id="I2">Department of Internal Medicine IV (Nephrology and Hypertension), Medical University Innsbruck, Innsbruck, Austria</nlm:aff><country xml:lang="fr">Autriche</country><wicri:regionArea>Department of Internal Medicine IV (Nephrology and Hypertension), Medical University Innsbruck, Innsbruck</wicri:regionArea><wicri:noRegion>Innsbruck</wicri:noRegion></affiliation></author><author><name sortKey="Park, Se Jin" sort="Park, Se Jin" uniqKey="Park S" first="Se Jin" last="Park">Se Jin Park</name><affiliation wicri:level="1"><nlm:aff id="I3">Department of Pediatrics, Ajou University Hospital, Ajou University School of Medicine, Suwon, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Pediatrics, Ajou University Hospital, Ajou University School of Medicine, Suwon</wicri:regionArea><wicri:noRegion>Suwon</wicri:noRegion></affiliation></author><author><name sortKey="Kim, Seong Heon" sort="Kim, Seong Heon" uniqKey="Kim S" first="Seong Heon" last="Kim">Seong Heon Kim</name><affiliation wicri:level="1"><nlm:aff id="I4">Department of Pediatrics, Pusan National University Children's Hospital, Yangsan, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Pediatrics, Pusan National University Children's Hospital, Yangsan</wicri:regionArea><wicri:noRegion>Yangsan</wicri:noRegion></affiliation></author><author><name 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Kim</name><affiliation wicri:level="1"><nlm:aff id="I8">Keimyung University College of Nursing, Daegu, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Keimyung University College of Nursing, Daegu</wicri:regionArea><wicri:noRegion>Daegu</wicri:noRegion></affiliation></author><author><name sortKey="Kim, Dong Soo" sort="Kim, Dong Soo" uniqKey="Kim D" first="Dong Soo" last="Kim">Dong Soo Kim</name><affiliation wicri:level="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><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="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><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="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><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="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></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="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation><affiliation wicri:level="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation><affiliation wicri:level="3"><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><placeName><settlement type="city">Séoul</settlement><region 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Metalloproteinase- (MMP-) 3 Levels and Systemic Lupus Erythematosus: A Meta-analysis</title><author><name sortKey="Lee, Jiwon M" sort="Lee, Jiwon M" uniqKey="Lee J" first="Jiwon M." last="Lee">Jiwon M. Lee</name><affiliation wicri:level="1"><nlm:aff id="I1">Department of Pediatrics, Chungnam National University Hospital, Daejeon, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Pediatrics, Chungnam National University Hospital, Daejeon</wicri:regionArea><wicri:noRegion>Daejeon</wicri:noRegion></affiliation></author><author><name sortKey="Kronbichler, Andreas" sort="Kronbichler, Andreas" uniqKey="Kronbichler A" first="Andreas" last="Kronbichler">Andreas Kronbichler</name><affiliation wicri:level="1"><nlm:aff id="I2">Department of Internal Medicine IV (Nephrology and Hypertension), Medical University Innsbruck, Innsbruck, Austria</nlm:aff><country xml:lang="fr">Autriche</country><wicri:regionArea>Department of Internal Medicine IV (Nephrology and Hypertension), Medical University Innsbruck, Innsbruck</wicri:regionArea><wicri:noRegion>Innsbruck</wicri:noRegion></affiliation></author><author><name sortKey="Park, Se Jin" sort="Park, Se Jin" uniqKey="Park S" first="Se Jin" last="Park">Se Jin Park</name><affiliation wicri:level="1"><nlm:aff id="I3">Department of Pediatrics, Ajou University Hospital, Ajou University School of Medicine, Suwon, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Pediatrics, Ajou University Hospital, Ajou University School of Medicine, Suwon</wicri:regionArea><wicri:noRegion>Suwon</wicri:noRegion></affiliation></author><author><name sortKey="Kim, Seong Heon" sort="Kim, Seong Heon" uniqKey="Kim S" first="Seong Heon" last="Kim">Seong Heon Kim</name><affiliation wicri:level="1"><nlm:aff id="I4">Department of Pediatrics, Pusan National University Children's Hospital, Yangsan, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Pediatrics, Pusan National University Children's Hospital, Yangsan</wicri:regionArea><wicri:noRegion>Yangsan</wicri:noRegion></affiliation></author><author><name sortKey="Han, Kyoung Hee" sort="Han, Kyoung Hee" uniqKey="Han K" first="Kyoung Hee" last="Han">Kyoung Hee Han</name><affiliation wicri:level="1"><nlm:aff id="I5">Department of Pediatrics, Jeju National University School of Medicine, Jeju, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Pediatrics, Jeju National University School of Medicine, Jeju</wicri:regionArea><wicri:noRegion>Jeju</wicri:noRegion></affiliation></author><author><name sortKey="Kang, Hee Gyung" sort="Kang, Hee Gyung" uniqKey="Kang H" first="Hee Gyung" last="Kang">Hee Gyung Kang</name><affiliation wicri:level="3"><nlm:aff id="I6">Department of Pediatrics, Seoul National University Children's Hospital, Seoul, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Pediatrics, Seoul National University Children's Hospital, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Ha, Il Soo" sort="Ha, Il Soo" uniqKey="Ha I" first="Il Soo" last="Ha">Il Soo Ha</name><affiliation wicri:level="3"><nlm:aff id="I6">Department of Pediatrics, Seoul National University Children's Hospital, Seoul, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Pediatrics, Seoul National University Children's Hospital, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Cheong, Hae Il" sort="Cheong, Hae Il" uniqKey="Cheong H" first="Hae Il" last="Cheong">Hae Il Cheong</name><affiliation wicri:level="3"><nlm:aff id="I6">Department of Pediatrics, Seoul National University Children's Hospital, Seoul, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Pediatrics, Seoul National University Children's Hospital, Seoul</wicri:regionArea><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Kim, Ki Hwan" sort="Kim, Ki Hwan" uniqKey="Kim K" first="Ki Hwan" last="Kim">Ki Hwan Kim</name><affiliation wicri:level="3"><nlm:aff id="I7">Department of Pediatrics, Incheon St. Mary's Hospital, The Catholic University of Korea, Seoul, Republic of Korea</nlm:aff><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><author><name sortKey="Kim, Gaeun" sort="Kim, Gaeun" uniqKey="Kim G" first="Gaeun" last="Kim">Gaeun Kim</name><affiliation wicri:level="1"><nlm:aff id="I8">Keimyung University College of Nursing, Daegu, Republic of Korea</nlm:aff><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Keimyung University College of Nursing, Daegu</wicri:regionArea><wicri:noRegion>Daegu</wicri:noRegion></affiliation></author><author><name sortKey="Kim, Dong Soo" sort="Kim, Dong Soo" uniqKey="Kim D" first="Dong Soo" last="Kim">Dong Soo Kim</name><affiliation wicri:level="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><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="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><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="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author><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="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></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="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation><affiliation wicri:level="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation><affiliation wicri:level="3"><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><placeName><settlement type="city">Séoul</settlement><region type="capital">Région capitale de Séoul</region></placeName></affiliation></author></analytic><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></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><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><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Cook, H T" uniqKey="Cook H">H. T. Cook</name></author><author><name sortKey="Botto, M" uniqKey="Botto M">M. Botto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kotajima, L" uniqKey="Kotajima L">L. Kotajima</name></author><author><name sortKey="Aotsuka, S" uniqKey="Aotsuka S">S. Aotsuka</name></author><author><name sortKey="Fujimani, M" uniqKey="Fujimani M">M. Fujimani</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zhu, Q Q" uniqKey="Zhu Q">Q. Q. 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<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><affiliations><list><country><li>Autriche</li><li>Corée du Sud</li></country><region><li>Région capitale de Séoul</li></region><settlement><li>Séoul</li></settlement></list><tree><country name="Corée du Sud"><noRegion><name sortKey="Lee, Jiwon M" sort="Lee, Jiwon M" uniqKey="Lee J" first="Jiwon M." last="Lee">Jiwon M. Lee</name></noRegion><name sortKey="Chae, Hyun Wook" sort="Chae, Hyun Wook" uniqKey="Chae H" first="Hyun Wook" last="Chae">Hyun Wook Chae</name><name sortKey="Cheong, Hae Il" sort="Cheong, Hae Il" uniqKey="Cheong H" first="Hae Il" last="Cheong">Hae Il Cheong</name><name sortKey="Ha, Il Soo" sort="Ha, Il Soo" uniqKey="Ha I" first="Il Soo" last="Ha">Il Soo Ha</name><name sortKey="Han, Kyoung Hee" sort="Han, Kyoung Hee" uniqKey="Han K" first="Kyoung Hee" last="Han">Kyoung Hee Han</name><name sortKey="Kang, Hee Gyung" sort="Kang, Hee Gyung" uniqKey="Kang H" first="Hee Gyung" last="Kang">Hee Gyung Kang</name><name sortKey="Kim, Dong Soo" sort="Kim, Dong Soo" uniqKey="Kim D" first="Dong Soo" last="Kim">Dong Soo Kim</name><name sortKey="Kim, Gaeun" sort="Kim, Gaeun" uniqKey="Kim G" first="Gaeun" last="Kim">Gaeun Kim</name><name sortKey="Kim, Ki Hwan" sort="Kim, Ki Hwan" uniqKey="Kim K" first="Ki Hwan" last="Kim">Ki Hwan Kim</name><name sortKey="Kim, Seong Heon" sort="Kim, Seong Heon" uniqKey="Kim S" first="Seong Heon" last="Kim">Seong Heon Kim</name><name sortKey="Lee, Chul Ho" sort="Lee, Chul Ho" uniqKey="Lee C" first="Chul Ho" last="Lee">Chul Ho Lee</name><name sortKey="Lee, Keum Hwa" sort="Lee, Keum Hwa" uniqKey="Lee K" first="Keum Hwa" last="Lee">Keum Hwa Lee</name><name sortKey="Park, Se Jin" sort="Park, Se Jin" uniqKey="Park S" first="Se Jin" last="Park">Se Jin Park</name><name sortKey="Shin, Jae Il" sort="Shin, Jae Il" uniqKey="Shin J" first="Jae Il" last="Shin">Jae Il Shin</name><name sortKey="Shin, Jae Il" sort="Shin, Jae Il" uniqKey="Shin J" first="Jae Il" last="Shin">Jae Il Shin</name><name sortKey="Shin, Jae Il" sort="Shin, Jae Il" uniqKey="Shin J" first="Jae Il" last="Shin">Jae Il Shin</name></country><country name="Autriche"><noRegion><name sortKey="Kronbichler, Andreas" sort="Kronbichler, Andreas" uniqKey="Kronbichler A" first="Andreas" last="Kronbichler">Andreas Kronbichler</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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