The Personal Human Oral Microbiome Obscures the Effects of Treatment on Periodontal Disease
Identifieur interne : 000056 ( Pmc/Checkpoint ); précédent : 000055; suivant : 000057The Personal Human Oral Microbiome Obscures the Effects of Treatment on Periodontal Disease
Auteurs : Karen Schwarzberg [États-Unis] ; Rosalin Le [États-Unis] ; Balambal Bharti [États-Unis] ; Suzanne Lindsay [États-Unis] ; Giorgio Casaburi [Italie] ; Francesco Salvatore [Italie] ; Mohamed H. Saber [États-Unis] ; Faisal Alonaizan [États-Unis] ; J Rgen Slots [États-Unis] ; Roberta A. Gottlieb [États-Unis] ; J. Gregory Caporaso [États-Unis] ; Scott T. Kelley [États-Unis]Source :
- PLoS ONE [ 1932-6203 ] ; 2014.
Abstract
Periodontitis is a progressive disease of the periodontium with a complex, polymicrobial etiology. Recent Next-Generation Sequencing (NGS) studies of the microbial diversity associated with periodontitis have revealed strong, community-level differences in bacterial assemblages associated with healthy or diseased periodontal sites. In this study, we used NGS approaches to characterize changes in periodontal pocket bacterial diversity after standard periodontal treatment. Despite consistent changes in the abundance of certain taxa in individuals whose condition improved with treatment, post-treatment samples retained the highest similarity to pre-treatment samples from the same individual. Deeper phylogenetic analysis of periodontal pathogen-containing genera
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DOI: 10.1371/journal.pone.0086708
PubMed: 24489772
PubMed Central: 3906071
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Saber</name><affiliation wicri:level="2"><nlm:aff id="aff5"><addr-line>Section of Endodontics, Herman Ostrow School of Dentistry of USC, Los Angeles, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Endodontics, Herman Ostrow School of Dentistry of USC, Los Angeles, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Alonaizan, Faisal" sort="Alonaizan, Faisal" uniqKey="Alonaizan F" first="Faisal" last="Alonaizan">Faisal Alonaizan</name><affiliation wicri:level="2"><nlm:aff id="aff5"><addr-line>Section of Endodontics, Herman Ostrow School of Dentistry of USC, Los Angeles, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Endodontics, Herman Ostrow School of Dentistry of USC, Los Angeles, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Slots, J Rgen" sort="Slots, J Rgen" uniqKey="Slots J" first="J Rgen" last="Slots">J Rgen Slots</name><affiliation wicri:level="2"><nlm:aff id="aff6"><addr-line>Professor of Dentistry and Microbiology, Herman Ostrow School of Dentistry of USC, Los Angeles, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Professor of Dentistry and Microbiology, Herman Ostrow School of Dentistry of USC, Los Angeles, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Gottlieb, Roberta A" sort="Gottlieb, Roberta A" uniqKey="Gottlieb R" first="Roberta A." last="Gottlieb">Roberta A. 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R" first="Rosalin" last="Le">Rosalin Le</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Biology, San Diego State University, San Diego, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, San Diego State University, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Bharti, Balambal" sort="Bharti, Balambal" uniqKey="Bharti B" first="Balambal" last="Bharti">Balambal Bharti</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Graduate School of Public Health, San Diego State University, San Diego, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Graduate School of Public Health, San Diego State University, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Lindsay, Suzanne" sort="Lindsay, Suzanne" uniqKey="Lindsay S" first="Suzanne" last="Lindsay">Suzanne Lindsay</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Graduate School of Public Health, San Diego State University, San Diego, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Graduate School of Public Health, San Diego State University, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Casaburi, Giorgio" sort="Casaburi, Giorgio" uniqKey="Casaburi G" first="Giorgio" last="Casaburi">Giorgio Casaburi</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>CEINGE-Biotecnologie Avanzate, Napoli, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>CEINGE-Biotecnologie Avanzate, Napoli</wicri:regionArea><wicri:noRegion>Napoli</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università di Napoli Federico II, Napoli, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università di Napoli Federico II, Napoli</wicri:regionArea><wicri:noRegion>Napoli</wicri:noRegion></affiliation></author><author><name sortKey="Salvatore, Francesco" sort="Salvatore, Francesco" uniqKey="Salvatore F" first="Francesco" last="Salvatore">Francesco Salvatore</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>CEINGE-Biotecnologie Avanzate, Napoli, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>CEINGE-Biotecnologie Avanzate, Napoli</wicri:regionArea><wicri:noRegion>Napoli</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università di Napoli Federico II, Napoli, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università di Napoli Federico II, Napoli</wicri:regionArea><wicri:noRegion>Napoli</wicri:noRegion></affiliation></author><author><name sortKey="Saber, Mohamed H" sort="Saber, Mohamed H" uniqKey="Saber M" first="Mohamed H." last="Saber">Mohamed H. Saber</name><affiliation wicri:level="2"><nlm:aff id="aff5"><addr-line>Section of Endodontics, Herman Ostrow School of Dentistry of USC, Los Angeles, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Endodontics, Herman Ostrow School of Dentistry of USC, Los Angeles, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Alonaizan, Faisal" sort="Alonaizan, Faisal" uniqKey="Alonaizan F" first="Faisal" last="Alonaizan">Faisal Alonaizan</name><affiliation wicri:level="2"><nlm:aff id="aff5"><addr-line>Section of Endodontics, Herman Ostrow School of Dentistry of USC, Los Angeles, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Endodontics, Herman Ostrow School of Dentistry of USC, Los Angeles, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Slots, J Rgen" sort="Slots, J Rgen" uniqKey="Slots J" first="J Rgen" last="Slots">J Rgen Slots</name><affiliation wicri:level="2"><nlm:aff id="aff6"><addr-line>Professor of Dentistry and Microbiology, Herman Ostrow School of Dentistry of USC, Los Angeles, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Professor of Dentistry and Microbiology, Herman Ostrow School of Dentistry of USC, Los Angeles, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Gottlieb, Roberta A" sort="Gottlieb, Roberta A" uniqKey="Gottlieb R" first="Roberta A." last="Gottlieb">Roberta A. Gottlieb</name><affiliation wicri:level="2"><nlm:aff id="aff7"><addr-line>BioScience Center, San Diego State University, San Diego, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>BioScience Center, San Diego State University, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Caporaso, J Gregory" sort="Caporaso, J Gregory" uniqKey="Caporaso J" first="J. Gregory" last="Caporaso">J. Gregory Caporaso</name><affiliation wicri:level="2"><nlm:aff id="aff8"><addr-line>Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona</wicri:regionArea><placeName><region type="state">Arizona</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff9"><addr-line>Institute for Genomics and Systems Biology, Argonne National Laboratory, Argonne, Illinois, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Institute for Genomics and Systems Biology, Argonne National Laboratory, Argonne, Illinois</wicri:regionArea><placeName><region type="state">Illinois</region></placeName></affiliation></author><author><name sortKey="Kelley, Scott T" sort="Kelley, Scott T" uniqKey="Kelley S" first="Scott T." last="Kelley">Scott T. Kelley</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Biology, San Diego State University, San Diego, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, San Diego State University, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</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>Periodontitis is a progressive disease of the periodontium with a complex, polymicrobial etiology. Recent Next-Generation Sequencing (NGS) studies of the microbial diversity associated with periodontitis have revealed strong, community-level differences in bacterial assemblages associated with healthy or diseased periodontal sites. In this study, we used NGS approaches to characterize changes in periodontal pocket bacterial diversity after standard periodontal treatment. Despite consistent changes in the abundance of certain taxa in individuals whose condition improved with treatment, post-treatment samples retained the highest similarity to pre-treatment samples from the same individual. Deeper phylogenetic analysis of periodontal pathogen-containing genera <italic>Prevotella</italic> and <italic>Fusobacterium</italic> found both unexpected diversity and differential treatment response among species. Our results highlight how understanding interpersonal variability among microbiomes is necessary for determining how polymicrobial diseases respond to treatment and disturbance.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Dentino, A" uniqKey="Dentino A">A Dentino</name></author><author><name sortKey="Lee, S" uniqKey="Lee S">S Lee</name></author><author><name sortKey="Mailhot, J" uniqKey="Mailhot J">J Mailhot</name></author><author><name sortKey="Hefti, Af" uniqKey="Hefti A">AF Hefti</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Teles, R" uniqKey="Teles R">R Teles</name></author><author><name sortKey="Teles, F" uniqKey="Teles F">F Teles</name></author><author><name sortKey="Frias Lopez, J" uniqKey="Frias Lopez J">J Frias-Lopez</name></author><author><name sortKey="Paster, B" uniqKey="Paster B">B Paster</name></author><author><name sortKey="Haffajee, A" uniqKey="Haffajee A">A 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24489772</article-id><article-id pub-id-type="pmc">3906071</article-id><article-id pub-id-type="publisher-id">PONE-D-13-40128</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0086708</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Computational Biology</subject><subj-group><subject>Biological Data Management</subject><subject>Genomics</subject><subject>Sequence Analysis</subject></subj-group></subj-group><subj-group><subject>Genomics</subject><subj-group><subject>Genome Databases</subject></subj-group></subj-group><subj-group><subject>Microbiology</subject><subj-group><subject>Bacterial Pathogens</subject><subject>Host-Pathogen Interaction</subject><subject>Medical Microbiology</subject><subject>Microbial Pathogens</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Medicine</subject><subj-group><subject>Oral Medicine</subject><subj-group><subject>Dentistry</subject><subject>Oral Diseases</subject></subj-group></subj-group><subj-group><subject>Public Health</subject></subj-group></subj-group></article-categories><title-group><article-title>The Personal Human Oral Microbiome Obscures the Effects of Treatment on Periodontal Disease</article-title><alt-title alt-title-type="running-head">Periodontal Treatment Effects on Oral Microbiome</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Schwarzberg</surname><given-names>Karen</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Le</surname><given-names>Rosalin</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bharti</surname><given-names>Balambal</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lindsay</surname><given-names>Suzanne</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Casaburi</surname><given-names>Giorgio</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Salvatore</surname><given-names>Francesco</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Saber</surname><given-names>Mohamed H.</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Alonaizan</surname><given-names>Faisal</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Slots</surname><given-names>Jørgen</given-names></name><xref ref-type="aff" rid="aff6"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gottlieb</surname><given-names>Roberta A.</given-names></name><xref ref-type="aff" rid="aff7"><sup>7</sup></xref></contrib><contrib contrib-type="author"><name><surname>Caporaso</surname><given-names>J. Gregory</given-names></name><xref ref-type="aff" rid="aff8"><sup>8</sup></xref><xref ref-type="aff" rid="aff9"><sup>9</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kelley</surname><given-names>Scott T.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Department of Biology, San Diego State University, San Diego, California, United States of America</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Graduate School of Public Health, San Diego State University, San Diego, California, United States of America</addr-line></aff><aff id="aff3"><label>3</label><addr-line>CEINGE-Biotecnologie Avanzate, Napoli, Italy</addr-line></aff><aff id="aff4"><label>4</label><addr-line>Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università di Napoli Federico II, Napoli, Italy</addr-line></aff><aff id="aff5"><label>5</label><addr-line>Section of Endodontics, Herman Ostrow School of Dentistry of USC, Los Angeles, California, United States of America</addr-line></aff><aff id="aff6"><label>6</label><addr-line>Professor of Dentistry and Microbiology, Herman Ostrow School of Dentistry of USC, Los Angeles, California, United States of America</addr-line></aff><aff id="aff7"><label>7</label><addr-line>BioScience Center, San Diego State University, San Diego, California, United States of America</addr-line></aff><aff id="aff8"><label>8</label><addr-line>Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, United States of America</addr-line></aff><aff id="aff9"><label>9</label><addr-line>Institute for Genomics and Systems Biology, Argonne National Laboratory, Argonne, Illinois, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Bereswill</surname><given-names>Stefan</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Charité-University Medicine Berlin, Germany</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>skelley@mail.sdsu.edu</email></corresp><fn fn-type="conflict"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: KS RL BB SL RAG JGC STK. Performed the experiments: KS RL. Analyzed the data: KS GC FS JGC STK. Contributed reagents/materials/analysis tools: MHS FA JS. Wrote the paper: KS SL JS RAG JGC STK.</p></fn></author-notes><pub-date pub-type="collection"><year>2014</year></pub-date><pub-date pub-type="epub"><day>29</day><month>1</month><year>2014</year></pub-date><volume>9</volume><issue>1</issue><elocation-id>e86708</elocation-id><history><date date-type="received"><day>25</day><month>9</month><year>2013</year></date><date date-type="accepted"><day>12</day><month>12</month><year>2013</year></date></history><permissions><copyright-year>2014</copyright-year><copyright-holder>Schwarzberg et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><abstract><p>Periodontitis is a progressive disease of the periodontium with a complex, polymicrobial etiology. Recent Next-Generation Sequencing (NGS) studies of the microbial diversity associated with periodontitis have revealed strong, community-level differences in bacterial assemblages associated with healthy or diseased periodontal sites. In this study, we used NGS approaches to characterize changes in periodontal pocket bacterial diversity after standard periodontal treatment. Despite consistent changes in the abundance of certain taxa in individuals whose condition improved with treatment, post-treatment samples retained the highest similarity to pre-treatment samples from the same individual. Deeper phylogenetic analysis of periodontal pathogen-containing genera <italic>Prevotella</italic> and <italic>Fusobacterium</italic> found both unexpected diversity and differential treatment response among species. Our results highlight how understanding interpersonal variability among microbiomes is necessary for determining how polymicrobial diseases respond to treatment and disturbance.</p></abstract><funding-group><funding-statement>This work received financial support from the following sources: NIH Grant U26IHS300292 (PI: Calac; Project Leader: Gottlieb); “Native American Research Centers for Health (NARCH5): Periodontal Disease, Atherosclerosis, and the Oral Microbiome”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><page-count count="8"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>Italie</li><li>États-Unis</li></country><region><li>Arizona</li><li>Californie</li><li>Illinois</li></region></list><tree><country name="États-Unis"><region name="Californie"><name sortKey="Schwarzberg, Karen" sort="Schwarzberg, Karen" uniqKey="Schwarzberg K" first="Karen" last="Schwarzberg">Karen Schwarzberg</name></region><name sortKey="Alonaizan, Faisal" sort="Alonaizan, Faisal" uniqKey="Alonaizan F" first="Faisal" last="Alonaizan">Faisal Alonaizan</name><name sortKey="Bharti, Balambal" sort="Bharti, Balambal" uniqKey="Bharti B" first="Balambal" last="Bharti">Balambal Bharti</name><name sortKey="Caporaso, J Gregory" sort="Caporaso, J Gregory" uniqKey="Caporaso J" first="J. Gregory" last="Caporaso">J. Gregory Caporaso</name><name sortKey="Caporaso, J Gregory" sort="Caporaso, J Gregory" uniqKey="Caporaso J" first="J. Gregory" last="Caporaso">J. Gregory Caporaso</name><name sortKey="Gottlieb, Roberta A" sort="Gottlieb, Roberta A" uniqKey="Gottlieb R" first="Roberta A." last="Gottlieb">Roberta A. Gottlieb</name><name sortKey="Kelley, Scott T" sort="Kelley, Scott T" uniqKey="Kelley S" first="Scott T." last="Kelley">Scott T. Kelley</name><name sortKey="Le, Rosalin" sort="Le, Rosalin" uniqKey="Le R" first="Rosalin" last="Le">Rosalin Le</name><name sortKey="Lindsay, Suzanne" sort="Lindsay, Suzanne" uniqKey="Lindsay S" first="Suzanne" last="Lindsay">Suzanne Lindsay</name><name sortKey="Saber, Mohamed H" sort="Saber, Mohamed H" uniqKey="Saber M" first="Mohamed H." last="Saber">Mohamed H. Saber</name><name sortKey="Slots, J Rgen" sort="Slots, J Rgen" uniqKey="Slots J" first="J Rgen" last="Slots">J Rgen Slots</name></country><country name="Italie"><noRegion><name sortKey="Casaburi, Giorgio" sort="Casaburi, Giorgio" uniqKey="Casaburi G" first="Giorgio" last="Casaburi">Giorgio Casaburi</name></noRegion><name sortKey="Casaburi, Giorgio" sort="Casaburi, Giorgio" uniqKey="Casaburi G" first="Giorgio" last="Casaburi">Giorgio Casaburi</name><name sortKey="Salvatore, Francesco" sort="Salvatore, Francesco" uniqKey="Salvatore F" first="Francesco" last="Salvatore">Francesco Salvatore</name><name sortKey="Salvatore, Francesco" sort="Salvatore, Francesco" uniqKey="Salvatore F" first="Francesco" last="Salvatore">Francesco Salvatore</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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