Intraindividual variation in core microbiota in peri-implantitis and periodontitis
Identifieur interne : 000071 ( Pmc/Curation ); précédent : 000070; suivant : 000072Intraindividual variation in core microbiota in peri-implantitis and periodontitis
Auteurs : Noriko Maruyama ; Fumito Maruyama ; Yasuo Takeuchi ; Chihiro Aikawa ; Yuichi Izumi ; Ichiro NakagawaSource :
- Scientific Reports [ 2045-2322 ] ; 2014.
Abstract
The oral microbiota change dramatically with each part of the oral cavity, even within the same mouth. Nevertheless, the microbiota associated with peri-implantitis and periodontitis have been considered the same. To improve our knowledge of the different communities of complex oral microbiota, we compared the microbial features between peri-implantitis and periodontitis in 20 patients with both diseases. Although the clinical symptoms of peri-implantitis were similar to those of periodontitis, the core microbiota of the diseases differed. Correlation analysis revealed the specific microbial co-occurrence patterns and found some of the species were associated with the clinical parameters in a disease-specific manner. The proportion of
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DOI: 10.1038/srep06602
PubMed: 25308100
PubMed Central: 4194447
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Intraindividual variation in core microbiota in peri-implantitis and periodontitis</title><author><name sortKey="Maruyama, Noriko" sort="Maruyama, Noriko" uniqKey="Maruyama N" first="Noriko" last="Maruyama">Noriko Maruyama</name><affiliation><nlm:aff id="a1"><institution>Department of Periodontology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University</institution></nlm:aff></affiliation></author><author><name sortKey="Maruyama, Fumito" sort="Maruyama, Fumito" uniqKey="Maruyama F" first="Fumito" last="Maruyama">Fumito Maruyama</name><affiliation><nlm:aff id="a2"><institution>Department of Microbiology, Graduate School of Medicine, Kyoto University</institution></nlm:aff></affiliation></author><author><name sortKey="Takeuchi, Yasuo" sort="Takeuchi, Yasuo" uniqKey="Takeuchi Y" first="Yasuo" last="Takeuchi">Yasuo Takeuchi</name><affiliation><nlm:aff id="a1"><institution>Department of Periodontology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University</institution></nlm:aff></affiliation></author><author><name sortKey="Aikawa, Chihiro" sort="Aikawa, Chihiro" uniqKey="Aikawa C" first="Chihiro" last="Aikawa">Chihiro Aikawa</name><affiliation><nlm:aff id="a2"><institution>Department of Microbiology, Graduate School of Medicine, Kyoto University</institution></nlm:aff></affiliation></author><author><name sortKey="Izumi, Yuichi" sort="Izumi, Yuichi" uniqKey="Izumi Y" first="Yuichi" last="Izumi">Yuichi Izumi</name><affiliation><nlm:aff id="a1"><institution>Department of Periodontology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University</institution></nlm:aff></affiliation></author><author><name sortKey="Nakagawa, Ichiro" sort="Nakagawa, Ichiro" uniqKey="Nakagawa I" first="Ichiro" last="Nakagawa">Ichiro Nakagawa</name><affiliation><nlm:aff id="a2"><institution>Department of Microbiology, Graduate School of Medicine, Kyoto University</institution></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25308100</idno><idno type="pmc">4194447</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4194447</idno><idno type="RBID">PMC:4194447</idno><idno type="doi">10.1038/srep06602</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000071</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000071</idno><idno type="wicri:Area/Pmc/Curation">000071</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000071</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Intraindividual variation in core microbiota in peri-implantitis and periodontitis</title><author><name sortKey="Maruyama, Noriko" sort="Maruyama, Noriko" uniqKey="Maruyama N" first="Noriko" last="Maruyama">Noriko Maruyama</name><affiliation><nlm:aff id="a1"><institution>Department of Periodontology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University</institution></nlm:aff></affiliation></author><author><name sortKey="Maruyama, Fumito" sort="Maruyama, Fumito" uniqKey="Maruyama F" first="Fumito" last="Maruyama">Fumito Maruyama</name><affiliation><nlm:aff id="a2"><institution>Department of Microbiology, Graduate School of Medicine, Kyoto University</institution></nlm:aff></affiliation></author><author><name sortKey="Takeuchi, Yasuo" sort="Takeuchi, Yasuo" uniqKey="Takeuchi Y" first="Yasuo" last="Takeuchi">Yasuo Takeuchi</name><affiliation><nlm:aff id="a1"><institution>Department of Periodontology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University</institution></nlm:aff></affiliation></author><author><name sortKey="Aikawa, Chihiro" sort="Aikawa, Chihiro" uniqKey="Aikawa C" first="Chihiro" last="Aikawa">Chihiro Aikawa</name><affiliation><nlm:aff id="a2"><institution>Department of Microbiology, Graduate School of Medicine, Kyoto University</institution></nlm:aff></affiliation></author><author><name sortKey="Izumi, Yuichi" sort="Izumi, Yuichi" uniqKey="Izumi Y" first="Yuichi" last="Izumi">Yuichi Izumi</name><affiliation><nlm:aff id="a1"><institution>Department of Periodontology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University</institution></nlm:aff></affiliation></author><author><name sortKey="Nakagawa, Ichiro" sort="Nakagawa, Ichiro" uniqKey="Nakagawa I" first="Ichiro" last="Nakagawa">Ichiro Nakagawa</name><affiliation><nlm:aff id="a2"><institution>Department of Microbiology, Graduate School of Medicine, Kyoto University</institution></nlm:aff></affiliation></author></analytic><series><title level="j">Scientific Reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The oral microbiota change dramatically with each part of the oral cavity, even within the same mouth. Nevertheless, the microbiota associated with peri-implantitis and periodontitis have been considered the same. To improve our knowledge of the different communities of complex oral microbiota, we compared the microbial features between peri-implantitis and periodontitis in 20 patients with both diseases. Although the clinical symptoms of peri-implantitis were similar to those of periodontitis, the core microbiota of the diseases differed. Correlation analysis revealed the specific microbial co-occurrence patterns and found some of the species were associated with the clinical parameters in a disease-specific manner. The proportion of <italic>Prevotella nigrescens</italic> was significantly higher in peri-implantitis than in periodontitis, while the proportions of <italic>Peptostreptococcaceae</italic> sp. and <italic>Desulfomicrobium orale</italic> were significantly higher in periodontitis than in peri-implantitis. The severity of the peri-implantitis was also species-associated, including with an uncultured <italic>Treponema</italic> sp. that correlated to 4 clinical parameters. These results indicate that peri-implantitis and periodontitis are both polymicrobial infections with different causative pathogens. Our study provides a framework for the ecologically different bacterial communities between peri-implantitis and periodontitis, and it will be useful for further studies to understand the complex microbiota and pathogenic mechanisms of oral polymicrobial diseases.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Dewhirst, F E" uniqKey="Dewhirst F">F. E. Dewhirst</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Seymour, G J" uniqKey="Seymour G">G. J. Seymour</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zhou, Y" uniqKey="Zhou Y">Y. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id><journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id><journal-title-group><journal-title>Scientific Reports</journal-title></journal-title-group><issn pub-type="epub">2045-2322</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25308100</article-id><article-id pub-id-type="pmc">4194447</article-id><article-id pub-id-type="pii">srep06602</article-id><article-id pub-id-type="doi">10.1038/srep06602</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Intraindividual variation in core microbiota in peri-implantitis and periodontitis</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Maruyama</surname><given-names>Noriko</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Maruyama</surname><given-names>Fumito</given-names></name><xref ref-type="corresp" rid="c1">a</xref><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Takeuchi</surname><given-names>Yasuo</given-names></name><xref ref-type="corresp" rid="c2">b</xref><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Aikawa</surname><given-names>Chihiro</given-names></name><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Izumi</surname><given-names>Yuichi</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Nakagawa</surname><given-names>Ichiro</given-names></name><xref ref-type="aff" rid="a2">2</xref></contrib><aff id="a1"><label>1</label><institution>Department of Periodontology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University</institution></aff><aff id="a2"><label>2</label><institution>Department of Microbiology, Graduate School of Medicine, Kyoto University</institution></aff></contrib-group><author-notes><corresp id="c1"><label>a</label><email>maruyama.fumito.5e@kyoto-u.ac.jp</email></corresp><corresp id="c2"><label>b</label><email>takeuchi.peri@tmd.ac.jp</email></corresp></author-notes><pub-date pub-type="epub"><day>13</day><month>10</month><year>2014</year></pub-date><pub-date pub-type="collection"><year>2014</year></pub-date><volume>4</volume><elocation-id>6602</elocation-id><history><date date-type="received"><day>24</day><month>04</month><year>2014</year></date><date date-type="accepted"><day>19</day><month>09</month><year>2014</year></date></history><permissions><copyright-statement>Copyright © 2014, Macmillan Publishers Limited. All rights reserved</copyright-statement><copyright-year>2014</copyright-year><copyright-holder>Macmillan Publishers Limited. All rights reserved</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 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 in order to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/">http://creativecommons.org/licenses/by-nc-nd/4.0/</ext-link></license-p></license></permissions><abstract><p>The oral microbiota change dramatically with each part of the oral cavity, even within the same mouth. Nevertheless, the microbiota associated with peri-implantitis and periodontitis have been considered the same. To improve our knowledge of the different communities of complex oral microbiota, we compared the microbial features between peri-implantitis and periodontitis in 20 patients with both diseases. Although the clinical symptoms of peri-implantitis were similar to those of periodontitis, the core microbiota of the diseases differed. Correlation analysis revealed the specific microbial co-occurrence patterns and found some of the species were associated with the clinical parameters in a disease-specific manner. The proportion of <italic>Prevotella nigrescens</italic> was significantly higher in peri-implantitis than in periodontitis, while the proportions of <italic>Peptostreptococcaceae</italic> sp. and <italic>Desulfomicrobium orale</italic> were significantly higher in periodontitis than in peri-implantitis. The severity of the peri-implantitis was also species-associated, including with an uncultured <italic>Treponema</italic> sp. that correlated to 4 clinical parameters. These results indicate that peri-implantitis and periodontitis are both polymicrobial infections with different causative pathogens. Our study provides a framework for the ecologically different bacterial communities between peri-implantitis and periodontitis, and it will be useful for further studies to understand the complex microbiota and pathogenic mechanisms of oral polymicrobial diseases.</p></abstract></article-meta></front><floats-group><fig id="f1"><label>Figure 1</label><caption><title>Circular maximum likelihood phylogenetic tree at the genus level.</title><p>The inner band shows the genera coloured by phylum (see key for taxa with multiple members). The outer bands show the relative abundance: red for peri-implantitis, blue for periodontitis, and green for overall relative abundance. The tree was constructed with the Interactive Tree of Life tool and the taxonomic names were based on results from the Ribosomal Database Project classifier. The statistical differences were calculated by Wilcoxon signed rank tests. *<italic>P</italic> <0.05 and q <0.1.</p></caption><graphic xlink:href="srep06602-f1"></graphic></fig><fig id="f2"><label>Figure 2</label><caption><title>Principal coordinate analysis (PCoA) and microbial differences at the species level.</title><p>(a) PCoA plots of the unweighted UniFrac distances for the samples by disease. (b) The most abundant species (>0.5% abundance) in the peri-implantitis and periodontitis samples. The species name or Human Oral Taxon (HOT) ID in the Human Oral Microbiome is shown. The taxonomy assignments were based on information in the Human Oral Microbiome Database, and the statistical differences were calculated by Wilcoxon signed rank tests. *<italic>P</italic> <0.05 and q <0.1.</p></caption><graphic xlink:href="srep06602-f2"></graphic></fig><fig id="f3"><label>Figure 3</label><caption><title>The microbiota associated with peri-implantitis.</title><p>(a) The core microbiota of peri-implantitis and periodontitis. The model includes the species detected at peri-implantitis (red), periodontitis (blue), and both sites (green), where the species were found in at least 50% of patients with a mean relative abundance of >1%, or were statistically different (outside of the square boxes; see <xref ref-type="fig" rid="f2">Figure 2b</xref>). The species detected in at least 80% of patients in both sites are indicated in bold. The inner box labelled with 1 indicates a mean relative abundance of ≥2% in periodontitis and <2% in periodontitis. The inner box labelled with 2 indicates a mean relative abundance of ≥2% in both sites. The inner box labelled with 3 indicates a mean relative abundance of <2% in periodontitis and ≥2% in periodontitis. The inner box labelled with 4 indicates a mean relative abundance of <2% in type of site. <italic>Peptostreptococcaceae</italic> [XI][G-4] sp. HOT369 is statistically abundant, although showed a mean relative abundance of <1% in periodontitis (see <xref ref-type="fig" rid="f2">Figure 2b</xref>). The species name or Human Oral Taxon (HOT) ID in the Human Oral Microbiome Database is shown. The statistical differences were calculated by Wilcoxon signed rank tests. *<italic>P</italic> <0.05 and q <0.1. (b) Bacterial taxa associated with the progression of peri-implantitis. The model represents all bacterial taxa associated with each of the four clinical parameters of peri-implantitis (<italic>P</italic> <0.05 and q <0.1). The species name or HOT ID is shown. The taxa correlated to four parameters (red box) and three parameters (black boxes) are shown. PPD, probing pocket depth; CAL, clinical attachment loss.</p></caption><graphic xlink:href="srep06602-f3"></graphic></fig><fig id="f4"><label>Figure 4</label><caption><title>Co-occurrence and co-exclusion analysis of the bacterial taxa.</title><p>Co-occurrence and co-exclusion were calculated by Spearman rank correlations between the abundant bacterial taxa. The co-occurrence of the top 30 species in the peri-implantitis and periodontitis samples is shown on the right and left, respectively. The species name or Human Oral Taxon ID in the Human Oral Microbiome Database is shown. The correlation values range from -1.00 (green) to 1.00 (red).</p></caption><graphic xlink:href="srep06602-f4"></graphic></fig><table-wrap position="float" id="t1"><label>Table 1</label><caption><title>Summary of meta-data on patients</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></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50">Peri-implantitis sites</th><th align="center" valign="top" charoff="50">Periodontitis sites</th><th align="center" valign="top" charoff="50"><italic>P</italic> value<xref ref-type="fn" rid="t1-fn2">a</xref></th></tr></thead><tbody valign="top"><tr><td align="justify" valign="top" charoff="50">Age</td><td colspan="2" align="center" valign="top" charoff="50">60.1 ± 1.7</td><td align="left" valign="top" charoff="50"> </td></tr><tr><td align="justify" valign="top" charoff="50">Gender</td><td colspan="2" align="center" valign="top" charoff="50">7 males, 13 females</td><td align="left" valign="top" charoff="50"> </td></tr><tr><td align="justify" valign="top" charoff="50">Smoking</td><td colspan="2" align="center" valign="top" charoff="50">6</td><td align="left" valign="top" charoff="50"> </td></tr><tr><td align="justify" valign="top" charoff="50">Maxillary anterior</td><td align="center" valign="top" charoff="50">7</td><td align="center" valign="top" charoff="50">5</td><td align="char" valign="top" char="." charoff="50">0.49</td></tr><tr><td align="justify" valign="top" charoff="50">Maxillary posterior</td><td align="center" valign="top" charoff="50">5</td><td align="center" valign="top" charoff="50">8</td><td align="char" valign="top" char="." charoff="50">0.33</td></tr><tr><td align="justify" valign="top" charoff="50">Mandibular anterior</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">2</td><td align="char" valign="top" char="." charoff="50">0.16</td></tr><tr><td align="justify" valign="top" charoff="50">Mandibular posterior</td><td align="center" valign="top" charoff="50">8</td><td align="center" valign="top" charoff="50">5</td><td align="char" valign="top" char="." charoff="50">0.33</td></tr><tr><td align="justify" valign="top" charoff="50">Years in function</td><td align="char" valign="top" char=" " charoff="50">5.7 ± 0.7</td><td align="left" valign="top" charoff="50"> </td><td align="left" valign="top" charoff="50"> </td></tr><tr><td align="justify" valign="top" charoff="50">PPD (sampled sites)<xref ref-type="fn" rid="t1-fn2">b</xref></td><td align="char" valign="top" char=" " charoff="50">7.0 ± 0.6 mm</td><td align="char" valign="top" char=" " charoff="50">5.5 ± 0.4 mm</td><td align="char" valign="top" char="." charoff="50"><0.05</td></tr><tr><td align="justify" valign="top" charoff="50">CAL (sampled sites)<xref ref-type="fn" rid="t1-fn3">c</xref></td><td align="char" valign="top" char=" " charoff="50">7.5 ± 0.6 mm</td><td align="char" valign="top" char=" " charoff="50">6.4 ± 0.4 mm</td><td align="char" valign="top" char="." charoff="50">0.09</td></tr><tr><td align="justify" valign="top" charoff="50">BOP (sampled sites)<xref ref-type="fn" rid="t1-fn3">d</xref></td><td align="center" valign="top" charoff="50">100%</td><td align="center" valign="top" charoff="50">100%</td><td align="left" valign="top" charoff="50"> </td></tr><tr><td align="justify" valign="top" charoff="50">Number of sites with pus</td><td align="center" valign="top" charoff="50">9</td><td align="center" valign="top" charoff="50">0</td><td align="char" valign="top" char="." charoff="50"><0.05</td></tr><tr><td align="justify" valign="top" charoff="50">Radiographic bone loss</td><td align="char" valign="top" char=" " charoff="50">45.2 ± 7.2%</td><td align="char" valign="top" char=" " charoff="50">42.9 ± 5.2%</td><td align="char" valign="top" char="." charoff="50">0.78</td></tr></tbody></table><table-wrap-foot><fn id="t1-fn1"><p>Numbers shown are mean ± s.d.</p></fn><fn id="t1-fn2"><p><sup>a</sup>Statistical differences were calculated using paired t-tests; <sup>b</sup>Probing pocket depth.</p></fn><fn id="t1-fn3"><p><sup>c</sup>Clinical attachment loss; <sup>d</sup>Bleeding on probing.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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