Marginal bone loss around non-submerged implants is associated with salivary microbiome during bone healing
Identifieur interne : 000822 ( Pmc/Curation ); précédent : 000821; suivant : 000823Marginal bone loss around non-submerged implants is associated with salivary microbiome during bone healing
Auteurs : Xiao-Bo Duan [République populaire de Chine] ; Ting-Xi Wu [États-Unis] ; Yu-Chen Guo [République populaire de Chine] ; Xue-Dong Zhou [République populaire de Chine] ; Yi-Ling Lei [République populaire de Chine] ; Xin Xu [République populaire de Chine] ; An-Chun Mo [République populaire de Chine] ; Yong-Yue Wang [République populaire de Chine] ; Quan Yuan [République populaire de Chine]Source :
- International Journal of Oral Science [ 1674-2818 ] ; 2017.
Abstract
Marginal bone loss during bone healing exists around non-submerged dental implants. The aim of this study was to identify the relationship between different degrees of marginal bone loss during bone healing and the salivary microbiome. One hundred patients were recruited, and marginal bone loss around their implants was measured using cone beam computed tomography during a 3-month healing period. The patients were divided into three groups according to the severity of marginal bone loss. Saliva samples were collected from all subjected and were analysed using 16S MiSeq sequencing. Although the overall structure of the microbial community was not dramatically altered, the relative abundance of several taxonomic groups noticeably changed. The abundance of species in the phyla
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DOI: 10.1038/ijos.2017.18
PubMed: 28621324
PubMed Central: 5518974
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of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Operative Dentistry and Endodontics, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Lei, Yi Ling" sort="Lei, Yi Ling" uniqKey="Lei Y" first="Yi-Ling" last="Lei">Yi-Ling Lei</name><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Department of Oral Implantology, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Xu, Xin" sort="Xu, Xin" uniqKey="Xu X" first="Xin" last="Xu">Xin Xu</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Operative Dentistry and Endodontics, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Mo, An Chun" sort="Mo, An Chun" uniqKey="Mo A" first="An-Chun" last="Mo">An-Chun Mo</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Department of Oral Implantology, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Wang, Yong Yue" sort="Wang, Yong Yue" uniqKey="Wang Y" first="Yong-Yue" last="Wang">Yong-Yue Wang</name><affiliation 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Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Department of Oral Implantology, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28621324</idno><idno type="pmc">5518974</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5518974</idno><idno type="RBID">PMC:5518974</idno><idno type="doi">10.1038/ijos.2017.18</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">000822</idno><idno 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sortKey="Wu, Ting Xi" sort="Wu, Ting Xi" uniqKey="Wu T" first="Ting-Xi" last="Wu">Ting-Xi Wu</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>School of Dentistry, University of California, Los Angeles</institution>, CA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Guo, Yu Chen" sort="Guo, Yu Chen" uniqKey="Guo Y" first="Yu-Chen" last="Guo">Yu-Chen Guo</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Zhou, Xue Dong" sort="Zhou, Xue Dong" uniqKey="Zhou X" first="Xue-Dong" last="Zhou">Xue-Dong Zhou</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Operative Dentistry and Endodontics, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Lei, Yi Ling" sort="Lei, Yi Ling" uniqKey="Lei Y" first="Yi-Ling" last="Lei">Yi-Ling Lei</name><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Department of Oral Implantology, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Xu, Xin" sort="Xu, Xin" uniqKey="Xu X" first="Xin" last="Xu">Xin Xu</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Operative Dentistry and Endodontics, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Mo, An Chun" sort="Mo, An Chun" uniqKey="Mo A" first="An-Chun" last="Mo">An-Chun Mo</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Department of Oral Implantology, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Wang, Yong Yue" sort="Wang, Yong Yue" uniqKey="Wang Y" first="Yong-Yue" last="Wang">Yong-Yue Wang</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Department of Oral Implantology, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Yuan, Quan" sort="Yuan, Quan" uniqKey="Yuan Q" first="Quan" last="Yuan">Quan Yuan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><institution>Department of Oral Implantology, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">International Journal of Oral Science</title><idno type="ISSN">1674-2818</idno><idno type="eISSN">2049-3169</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Marginal bone loss during bone healing exists around non-submerged dental implants. The aim of this study was to identify the relationship between different degrees of marginal bone loss during bone healing and the salivary microbiome. One hundred patients were recruited, and marginal bone loss around their implants was measured using cone beam computed tomography during a 3-month healing period. The patients were divided into three groups according to the severity of marginal bone loss. Saliva samples were collected from all subjected and were analysed using 16S MiSeq sequencing. Although the overall structure of the microbial community was not dramatically altered, the relative abundance of several taxonomic groups noticeably changed. The abundance of species in the phyla <italic>Spirochaeta</italic> and <italic>Synergistetes</italic> increased significantly as the bone loss became more severe. Species within the genus <italic>Treponema</italic> also exhibited increased abundance, whereas <italic>Veillonella</italic>, <italic>Haemophilus</italic> and <italic>Leptotrichia</italic> exhibited reduced abundances, in groups with more bone loss. <italic>Porphyromonasgingivalis</italic>, <italic>Treponemadenticola</italic> and <italic>Streptococcus intermedius</italic> were significantly more abundant in the moderate group and/or severe group. The severity of marginal bone loss around the non-submerged implant was associated with dissimilar taxonomic compositions. An increased severity of marginal bone loss was related to increased proportions of periodontal pathogenic species. These data suggest a potential role of microbes in the progression of marginal bone loss during bone healing.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Oral Sci</journal-id><journal-id journal-id-type="iso-abbrev">Int J Oral Sci</journal-id><journal-title-group><journal-title>International Journal of Oral Science</journal-title></journal-title-group><issn pub-type="ppub">1674-2818</issn><issn pub-type="epub">2049-3169</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28621324</article-id><article-id pub-id-type="pmc">5518974</article-id><article-id pub-id-type="pii">ijos201718</article-id><article-id pub-id-type="doi">10.1038/ijos.2017.18</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject></subj-group></article-categories><title-group><article-title>Marginal bone loss around non-submerged implants is associated with salivary microbiome during bone healing</article-title><alt-title alt-title-type="running">Marginal bone loss and the salivary microbiome</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Duan</surname><given-names>Xiao-Bo</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Wu</surname><given-names>Ting-Xi</given-names></name><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Guo</surname><given-names>Yu-Chen</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Zhou</surname><given-names>Xue-Dong</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Lei</surname><given-names>Yi-Ling</given-names></name><xref ref-type="aff" rid="aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Xu</surname><given-names>Xin</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Mo</surname><given-names>An-Chun</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Yong-Yue</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Yuan</surname><given-names>Quan</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff4">4</xref><xref ref-type="corresp" rid="caf1">*</xref></contrib><aff id="aff1"><label>1</label><institution>State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></aff><aff id="aff2"><label>2</label><institution>School of Dentistry, University of California, Los Angeles</institution>, CA,<country>USA</country></aff><aff id="aff3"><label>3</label><institution>Department of Operative Dentistry and Endodontics, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></aff><aff id="aff4"><label>4</label><institution>Department of Oral Implantology, West China Hospital of Stomatology, Sichuan University</institution>, Chengdu,<country>China</country></aff></contrib-group><author-notes><corresp id="caf1"><label>*</label><institution>State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University</institution>, No. 14, Section 3, Renmin South Road, Chengdu 610041, <country>China</country> E-mail: <email>yuanquan@scu.edu.cn</email></corresp></author-notes><pub-date pub-type="ppub"><month>06</month><year>2017</year></pub-date><pub-date pub-type="epub"><day>16</day><month>06</month><year>2017</year></pub-date><pub-date pub-type="pmc-release"><day>1</day><month>6</month><year>2017</year></pub-date><volume>9</volume><issue>2</issue><fpage>95</fpage><lpage>103</lpage><history><date date-type="accepted"><day>28</day><month>03</month><year>2017</year></date></history><permissions><copyright-statement>Copyright © 2017 The Author(s)</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>The Author(s)</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International 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/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link></license-p></license></permissions><abstract><p>Marginal bone loss during bone healing exists around non-submerged dental implants. The aim of this study was to identify the relationship between different degrees of marginal bone loss during bone healing and the salivary microbiome. One hundred patients were recruited, and marginal bone loss around their implants was measured using cone beam computed tomography during a 3-month healing period. The patients were divided into three groups according to the severity of marginal bone loss. Saliva samples were collected from all subjected and were analysed using 16S MiSeq sequencing. Although the overall structure of the microbial community was not dramatically altered, the relative abundance of several taxonomic groups noticeably changed. The abundance of species in the phyla <italic>Spirochaeta</italic> and <italic>Synergistetes</italic> increased significantly as the bone loss became more severe. Species within the genus <italic>Treponema</italic> also exhibited increased abundance, whereas <italic>Veillonella</italic>, <italic>Haemophilus</italic> and <italic>Leptotrichia</italic> exhibited reduced abundances, in groups with more bone loss. <italic>Porphyromonasgingivalis</italic>, <italic>Treponemadenticola</italic> and <italic>Streptococcus intermedius</italic> were significantly more abundant in the moderate group and/or severe group. The severity of marginal bone loss around the non-submerged implant was associated with dissimilar taxonomic compositions. An increased severity of marginal bone loss was related to increased proportions of periodontal pathogenic species. These data suggest a potential role of microbes in the progression of marginal bone loss during bone healing.</p></abstract><kwd-group><kwd>dental implant</kwd><kwd>illumina sequencing</kwd><kwd>marginal bone loss</kwd><kwd>oral microbiome</kwd><kwd>peri-implantitis</kwd></kwd-group></article-meta></front><floats-group><fig id="fig1"><label>Figure 1</label><caption><p><bold>Microbial differences among the normal, moderate and severe groups at the genus level.</bold> The graph presents levels for the genera for which the abundances were ≥0.1% different between groups. The taxa were sorted according to the magnitude of change.</p></caption><graphic xlink:href="ijos201718f1"></graphic></fig><fig id="fig2"><label>Figure 2</label><caption><p><bold>Genera for which the abundances significantly differed between the groups.</bold> ANOVA (one-way) and <italic>post hoc</italic> least significant difference (LSD) were performed for multiple comparisons between the three different groups. *<italic>P</italic><0.05 between severe group and normal group; <sup>#</sup><italic>P</italic><0.05 between moderate group and normal group.</p></caption><graphic xlink:href="ijos201718f2"></graphic></fig><fig id="fig3"><label>Figure 3</label><caption><p><bold>NMDS analysis.</bold> NMDS based on the Bray–Curtis distance among all the three groups, and between the normal group and moderate or severe groups.</p></caption><graphic xlink:href="ijos201718f3"></graphic></fig><fig id="fig4"><label>Figure 4</label><caption><p><bold>Microbial differences among the normal, moderate and severe groups at the species level.</bold> The graph presents the most abundant species (≥0.5% abundance) in the normal, moderate and severe samples. The taxa were sorted according to the magnitude of change. The species name or human oral taxon ID in the human oral microbiome is presented.</p></caption><graphic xlink:href="ijos201718f4"></graphic></fig><fig id="fig5"><label>Figure 5</label><caption><p><bold>Species for which the abundances significantly differed between the groups.</bold> ANOVA (one-way) and <italic>post hoc</italic> least significant difference (LSD) were performed for multiple comparisons between the three different groups. *<italic>P</italic><0.05 between severe group and normal group; **<italic>P</italic><0.05 between severe group and moderate group; <sup>#</sup><italic>P</italic><0.05 between moderate group and normal group.</p></caption><graphic xlink:href="ijos201718f5"></graphic></fig><table-wrap id="tbl1"><label>Table 1</label><caption><title>Demographics and clinical parameters of all subjects</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50"> </th><th colspan="6" align="center" valign="top" charoff="50">Groups<hr></hr></th></tr><tr><th align="left" valign="top" charoff="50"> </th><th colspan="2" align="center" valign="top" charoff="50">Normal (<italic>n</italic>=28)<hr></hr></th><th colspan="2" align="center" valign="top" charoff="50">Moderate (<italic>n</italic>=36)<hr></hr></th><th colspan="2" align="center" valign="top" charoff="50">Severe (<italic>n</italic>=36)<hr></hr></th></tr><tr><th align="left" valign="top" charoff="50">Characteristics</th><th align="center" valign="top" charoff="50">T<sub>0</sub></th><th align="center" valign="top" charoff="50">T<sub>3</sub></th><th align="center" valign="top" charoff="50">T<sub>0</sub></th><th align="center" valign="top" charoff="50">T<sub>3</sub></th><th align="center" valign="top" charoff="50">T<sub>0</sub></th><th align="center" valign="top" charoff="50">T<sub>3</sub></th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">Male/Female</td><td align="center" valign="top" charoff="50">12/16</td><td align="center" valign="top" charoff="50">—</td><td align="center" valign="top" charoff="50">16/20</td><td align="center" valign="top" charoff="50">—</td><td align="center" valign="top" charoff="50">18/18</td><td align="center" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50">Age (mean±s.d.)</td><td align="char" valign="top" char="±" charoff="50">42.0±14.6</td><td align="center" valign="top" charoff="50">—</td><td align="char" valign="top" char="±" charoff="50">45.0±14.1</td><td align="center" valign="top" charoff="50">—</td><td align="char" valign="top" char="±" charoff="50">52.3±15.9</td><td align="center" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50">Alcohol drinking</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">Number of teeth (mean±s.d.)</td><td align="char" valign="top" char="±" charoff="50">28.05±2.25</td><td align="center" valign="top" charoff="50">—</td><td align="char" valign="top" char="±" charoff="50">28.42±1.77</td><td align="center" valign="top" charoff="50">—</td><td align="char" valign="top" char="±" charoff="50">27.34±2.58</td><td align="center" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50">Plaque index (mean±s.d.)</td><td align="char" valign="top" char="±" charoff="50">1.21±0.61</td><td align="char" valign="top" char="±" charoff="50">1.20±0.60</td><td align="char" valign="top" char="±" charoff="50">1.39±0.60</td><td align="char" valign="top" char="±" charoff="50">1.39±0.54</td><td align="char" valign="top" char="±" charoff="50">1.44±0.69</td><td align="char" valign="top" char="±" charoff="50">1.42±0.68</td></tr><tr><td align="left" valign="top" charoff="50">Gingival index (mean±s.d.)</td><td align="char" valign="top" char="±" charoff="50">1.08±0.54</td><td align="char" valign="top" char="±" charoff="50">1.06±0.52</td><td align="char" valign="top" char="±" charoff="50">1.28±0.50</td><td align="char" valign="top" char="±" charoff="50">1.24±0.51</td><td align="char" valign="top" char="±" charoff="50">1.40±0.50</td><td align="char" valign="top" char="±" charoff="50">1.35±0.54</td></tr><tr><td align="left" valign="top" charoff="50">Probing depth, mm (mean±s.d.)</td><td align="char" valign="top" char="±" charoff="50">2.02±0.73</td><td align="char" valign="top" char="±" charoff="50">2.01±0.69</td><td align="char" valign="top" char="±" charoff="50">2.25±0.60</td><td align="char" valign="top" char="±" charoff="50">2.20±0.54</td><td align="char" valign="top" char="±" charoff="50">2.51±1.44</td><td align="char" valign="top" char="±" charoff="50">2.33±1.39</td></tr><tr><td align="left" valign="top" charoff="50">MBL, mm (mean±s.d.)</td><td colspan="2" align="center" valign="top" charoff="50">0.28±0.13</td><td colspan="2" align="center" valign="top" charoff="50">0.71±0.13</td><td colspan="2" align="center" valign="top" charoff="50">1.55±0.53</td></tr></tbody></table><table-wrap-foot><fn id="t1-fn1"><p>T<sub>0</sub>: baseline (recruitment).</p></fn><fn id="t1-fn2"><p>T<sub>3</sub>: 3 months after implant surgery.</p></fn><fn id="t1-fn3"><p>s.d., standard deviation.</p></fn></table-wrap-foot></table-wrap><table-wrap id="tbl2"><label>Table 2</label><caption><title>The relative abundance (mean±s.e.m.) of the bacterial phylum among the normal, moderate and severe groups</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50"> </th><th colspan="3" align="center" valign="top" charoff="50">Groups</th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50">Intergroup</th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">Phyla</td><td align="center" valign="top" charoff="50">Normal (<italic>n</italic>=28)</td><td align="center" valign="top" charoff="50">Moderate (<italic>n</italic>=36)</td><td align="center" valign="top" charoff="50">Severe (<italic>n</italic>=36)</td><td align="center" valign="top" charoff="50"><italic>P</italic> value</td><td align="center" valign="top" charoff="50"><italic>P</italic><0.05</td></tr><tr><td align="left" valign="top" charoff="50"><italic>Firmicutes</italic></td><td align="char" valign="top" char="±" charoff="50">44.69±3.21</td><td align="char" valign="top" char="±" charoff="50">49.52±2.64</td><td align="char" valign="top" char="±" charoff="50">45.88±2.93</td><td align="char" valign="top" char="." charoff="50">0.478</td><td align="center" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"><italic>Proteobacteria</italic></td><td align="char" valign="top" char="±" charoff="50">27.66±3.71</td><td align="char" valign="top" char="±" charoff="50">25.66±3.13</td><td align="char" valign="top" char="±" charoff="50">27.63±3.57</td><td align="char" valign="top" char="." charoff="50">0.893</td><td align="center" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"><italic>Bacteroidetes</italic></td><td align="char" valign="top" char="±" charoff="50">14.01±1.75</td><td align="char" valign="top" char="±" charoff="50">12.31±1.67</td><td align="char" valign="top" char="±" charoff="50">13.30±1.72</td><td align="char" valign="top" char="." charoff="50">0.790</td><td align="center" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"><italic>Actinobacteria</italic></td><td align="char" valign="top" char="±" charoff="50">7.80±1.28</td><td align="char" valign="top" char="±" charoff="50">7.25±0.74</td><td align="char" valign="top" char="±" charoff="50">7.02±0.98</td><td align="char" valign="top" char="." charoff="50">0.861</td><td align="center" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"><italic>Fusobacteria</italic></td><td align="char" valign="top" char="±" charoff="50">4.20±0.63</td><td align="char" valign="top" char="±" charoff="50">2.85±0.39</td><td align="char" valign="top" char="±" charoff="50">3.29±0.59</td><td align="char" valign="top" char="." charoff="50">0.225</td><td align="center" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"><italic>Spirochaetae</italic></td><td align="char" valign="top" char="±" charoff="50">0.29±0.07</td><td align="char" valign="top" char="±" charoff="50">0.69±0.12</td><td align="char" valign="top" char="±" charoff="50">0.82±0.32</td><td align="char" valign="top" char="." charoff="50">0.046</td><td align="center" valign="top" charoff="50">M <italic>vs</italic> N</td></tr><tr><td align="left" valign="top" charoff="50"><italic>Synergistetes</italic></td><td align="char" valign="top" char="±" charoff="50">0.25±0.08</td><td align="char" valign="top" char="±" charoff="50">0.60±0.16</td><td align="char" valign="top" char="±" charoff="50">0.81±0.12</td><td align="char" valign="top" char="." charoff="50">0.035</td><td align="center" valign="top" charoff="50">S <italic>vs</italic> N</td></tr><tr><td align="left" valign="top" charoff="50"><italic>TM7</italic></td><td align="char" valign="top" char="±" charoff="50">0.43±0.15</td><td align="char" valign="top" char="±" charoff="50">0.54±0.15</td><td align="char" valign="top" char="±" charoff="50">0.60±0.28</td><td align="char" valign="top" char="." charoff="50">0.864</td><td align="center" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50">The others</td><td align="char" valign="top" char="±" charoff="50">0.67±0.18</td><td align="char" valign="top" char="±" charoff="50">0.60±0.12</td><td align="char" valign="top" char="±" charoff="50">0.66±0.12</td><td align="center" valign="top" charoff="50">0.739</td><td align="center" valign="top" charoff="50">—</td></tr></tbody></table><table-wrap-foot><fn id="t2-fn1"><p>M, moderate group; N, normal group; S, severe group; s.e.m., standard error of the mean.</p></fn><fn id="t2-fn2"><p>ANOVA (one-way) and <italic>post hoc</italic> least significant difference (LSD) were performed for multiple comparisons between the three different niches. The significance threshold was set at 0.05.</p></fn></table-wrap-foot></table-wrap><table-wrap id="tbl3"><label>Table 3</label><caption><title>The relative abundance (mean±s.e.m.) of the species associated with disease among the normal, moderate and severe groups</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="char" char="±"></col><col align="char" char="±"></col><col align="char" char="±"></col><col align="char" char="."></col><col align="left"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50"> </th><th colspan="3" align="center" valign="top" char="±" charoff="50">Groups<hr></hr></th><th align="center" valign="top" char="." charoff="50"> </th><th align="center" valign="top" charoff="50">Intergroup</th></tr><tr><th align="left" valign="top" charoff="50">Species</th><th align="center" valign="top" char="±" charoff="50">Normal (<italic>n</italic>=28)</th><th align="center" valign="top" char="±" charoff="50">Moderate (<italic>n</italic>=36)</th><th align="center" valign="top" char="±" charoff="50">Severe (<italic>n</italic>=36)</th><th align="char" valign="top" char="." charoff="50"><italic>P</italic> value</th><th align="center" valign="top" charoff="50"><italic>P</italic><0.05</th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50"> </td><td align="char" valign="top" char="±" charoff="50"> </td><td colspan="2" align="center" valign="top" char="±" charoff="50">Red complex</td><td align="char" valign="top" char="." charoff="50"> </td><td align="left" valign="top" charoff="50"> </td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Porphyromonas gingivali</italic></td><td align="char" valign="top" char="±" charoff="50">0.25±0.12</td><td align="char" valign="top" char="±" charoff="50">0.38±0.11</td><td align="char" valign="top" char="±" charoff="50">1.29±0.43</td><td align="char" valign="top" char="." charoff="50">0.020</td><td align="left" valign="top" charoff="50">S <italic>vs</italic> N; S <italic>vs</italic> M</td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Tannerella forsythia</italic></td><td align="char" valign="top" char="±" charoff="50">0.13±0.04</td><td align="char" valign="top" char="±" charoff="50">0.12±0.02</td><td align="char" valign="top" char="±" charoff="50">0.20±0.04</td><td align="char" valign="top" char="." charoff="50">0.223</td><td align="left" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Treponema denticola</italic></td><td align="char" valign="top" char="±" charoff="50">0.03±0.01</td><td align="char" valign="top" char="±" charoff="50">0.05±0.01</td><td align="char" valign="top" char="±" charoff="50">0.09±0.01</td><td align="char" valign="top" char="." charoff="50">0.046</td><td align="left" valign="top" charoff="50">M <italic>vs</italic> N</td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Eubacterium nodatum</italic></td><td align="char" valign="top" char="±" charoff="50">0.03±0.01</td><td align="char" valign="top" char="±" charoff="50">0.07±0.02</td><td align="char" valign="top" char="±" charoff="50">0.07±0.03</td><td align="char" valign="top" char="." charoff="50">0.349</td><td align="left" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Treponema socranskii</italic></td><td align="char" valign="top" char="±" charoff="50">0.03±0.01</td><td align="char" valign="top" char="±" charoff="50">0.06±0.02</td><td align="char" valign="top" char="±" charoff="50">0.09±0.05</td><td align="char" valign="top" char="." charoff="50">0.441</td><td align="left" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"> </td><td> </td><td> </td><td> </td><td> </td><td> </td></tr><tr><td align="left" valign="top" charoff="50"> </td><td align="char" valign="top" char="±" charoff="50"> </td><td colspan="2" align="center" valign="top" char="±" charoff="50">Orange complex</td><td align="char" valign="top" char="." charoff="50"> </td><td align="left" valign="top" charoff="50"> </td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Prevotella melaninogenica</italic></td><td align="char" valign="top" char="±" charoff="50">4.65±0.90</td><td align="char" valign="top" char="±" charoff="50">3.31±0.84</td><td align="char" valign="top" char="±" charoff="50">3.18±0.76</td><td align="char" valign="top" char="." charoff="50">0.420</td><td align="left" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Prevotella intermedia</italic></td><td align="char" valign="top" char="±" charoff="50">0.41±0.10</td><td align="char" valign="top" char="±" charoff="50">0.34±0.09</td><td align="char" valign="top" char="±" charoff="50">0.47±0.16</td><td align="char" valign="top" char="." charoff="50">0.757</td><td align="left" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Prevotella nigrescens</italic></td><td align="char" valign="top" char="±" charoff="50">0.05±0.02</td><td align="char" valign="top" char="±" charoff="50">0.06±0.02</td><td align="char" valign="top" char="±" charoff="50">0.05±0.03</td><td align="char" valign="top" char="." charoff="50">0.969</td><td align="left" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Fusobacterium nucleatum</italic> subsp. <italic>vincentii</italic></td><td align="char" valign="top" char="±" charoff="50">0.57±0.12</td><td align="char" valign="top" char="±" charoff="50">0.72±0.15</td><td align="char" valign="top" char="±" charoff="50">0.74±0.15</td><td align="char" valign="top" char="." charoff="50">0.688</td><td align="left" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Fusobacterium periodonticum</italic></td><td align="char" valign="top" char="±" charoff="50">1.62±0.29</td><td align="char" valign="top" char="±" charoff="50">0.92±0.16</td><td align="char" valign="top" char="±" charoff="50">1.60±0.40</td><td align="char" valign="top" char="." charoff="50">0.164</td><td align="left" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"> </td><td> </td><td> </td><td> </td><td> </td><td> </td></tr><tr><td align="left" valign="top" charoff="50"> </td><td align="char" valign="top" char="±" charoff="50"> </td><td colspan="2" align="center" valign="top" char="±" charoff="50">Yellow complex</td><td align="char" valign="top" char="." charoff="50"> </td><td align="left" valign="top" charoff="50"> </td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Streptococcus sanguinis</italic></td><td align="char" valign="top" char="±" charoff="50">1.42±0.28</td><td align="char" valign="top" char="±" charoff="50">1.97±0.39</td><td align="char" valign="top" char="±" charoff="50">1.57±0.43</td><td align="char" valign="top" char="." charoff="50">0.593</td><td align="left" valign="top" charoff="50">—</td></tr><tr><td align="left" valign="top" charoff="50"> <italic>Streptococcus intermedius</italic></td><td align="char" valign="top" char="±" charoff="50">0.12±0.03</td><td align="char" valign="top" char="±" charoff="50">0.28±0.06</td><td align="char" valign="top" char="±" charoff="50">0.42±0.07</td><td align="char" valign="top" char="." charoff="50">0.045</td><td align="left" valign="top" charoff="50">S <italic>vs</italic> N; M <italic>vs</italic> N</td></tr></tbody></table><table-wrap-foot><fn id="t3-fn1"><p>M, moderate group; N, normal group; S, severe group; s.e.m., standard error of the mean.</p></fn><fn id="t3-fn2"><p>ANOVA (one-way) and <italic>post hoc</italic> least significant difference (LSD) were performed for multiple comparisons between the three different groups. 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