{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T06:01:17Z","timestamp":1789624877460,"version":"build-2803163510"},"reference-count":53,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,8,29]],"date-time":"2024-08-29T00:00:00Z","timestamp":1724889600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100009504","name":"School of Stomatology, Peking University","doi-asserted-by":"publisher","award":["2022-PT-06, No. 82201022, No. ZDYF2021SHFZ229, 3030546840026,  82301072,  2021002"],"award-info":[{"award-number":["2022-PT-06, No. 82201022, No. ZDYF2021SHFZ229, 3030546840026,  82301072,  2021002"]}],"id":[{"id":"10.13039\/501100009504","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:sec><jats:title>Objective<\/jats:title><jats:p>The purpose of this systematic bioinformatics analysis was to describe the compositions and differences in submucosal microbial profiles of peri-implants\u2019 diseases and healthy implant.<\/jats:p><\/jats:sec><jats:sec><jats:title>Material and methods<\/jats:title><jats:p>PubMed, Embase, ETH Z, Scopus, CNKI, and Wanfang databases were searched to screen relevant literature on the analysis of peri-implant microflora based on the sequencing analysis technique of 16S ribosomal RNA (16S rRNA) gene. High-throughput sequencing of the 16S rRNA gene of microorganisms from healthy implants, peri-implant mucositis, and peri-implantitis was downloaded from the screened articles. EasyAmplicon and Usearch global algorithm were used to match the reads from each dataset to a full length of 16S rRNA or ITS gene sequence. The microorganisms based on the Human Oral Microbiome Database (HOMD) were re-classified, and the microbial diversity, flora composition, and differential species of the samples were re-analyzed, including taxonomic classification and alpha and beta diversity calculations. The co-occurrence network was also re-analyzed.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>A total of seven articles with 240 implants were included. Among them, 51 were healthy implants (HI), 43 were in the peri-implant mucositis (PM) group, and 146 were in the peri-implantitis (PI) group. A total of 26,483 OTUs were obtained, and 877 microorganisms were annotated. The alpha diversity including Chao1 (healthy implants, 121.04 \u00b1 92.76; peri-implant mucositis, 128.21 \u00b1 66.77; peri-implantitis, 131.15 \u00b1 84.69) and Shannon (healthy implants, 3.25 \u00b1 0.65; peri-implant mucositis, 3.73 \u00b1 0.61; peri-implantitis, 3.53 \u00b1 0.67) of the samples from the three groups showed a significant difference. The beta diversity of the three samples was statistically different among groups. The genera of <jats:italic>Treponema<\/jats:italic> and <jats:italic>Fretibacterium<\/jats:italic> were significantly more abundant in the PI group than in the other two groups, and the genus of <jats:italic>Streptococcus<\/jats:italic> was more abundant in the HI group. The relative abundance of <jats:italic>Porphyromonas<\/jats:italic> in the peri-implantitis group was 6.1%. The results of the co-occurrence network showed differences in the network topology among the three groups of samples. The most connected three genera in the healthy implants were <jats:italic>Halomonas<\/jats:italic>, <jats:italic>Fusobacterium<\/jats:italic>, and <jats:italic>Fretibacterium<\/jats:italic>. The most connected three genera in peri-implant mucositis were <jats:italic>Alistipes<\/jats:italic>, <jats:italic>Clostridia UCG-014<\/jats:italic>, and <jats:italic>Candidatus Saccharimonas<\/jats:italic>. The most connected three genera in the peri-implantitis group were <jats:italic>Lachnoanaerobaculum<\/jats:italic>, <jats:italic>Fusobacterium<\/jats:italic>, and <jats:italic>Atopobium<\/jats:italic>. The betweenness of <jats:italic>Porphvromonas gingivalis<\/jats:italic> (red complex) in the PI group (7,900) was higher than in the HI group (23).<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>The community compositions of peri-implant submucosal microorganisms were significantly different in healthy implants, peri-implant mucositis, and peri-implantitis. The submucosal microbial communities in peri-implantitis were characterized by high species richness and diversity compared with the healthy implants; the relative abundance of red complex, some members of the yellow complex, and some novel periodontal pathogens was higher in the peri-implantitis and peri-implant mucositis groups than in the healthy implant group. The core flora of the co-occurrence network of healthy implants, peri-implant mucositis, and peri-implantitis varied considerably. The peri-implantitis site presented a relative disequilibrium microbial community, and <jats:italic>Porphyromonas<\/jats:italic> may play an important role in the co-occurrence network.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fcimb.2024.1445751","type":"journal-article","created":{"date-parts":[[2024,8,29]],"date-time":"2024-08-29T05:10:15Z","timestamp":1724908215000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":17,"title":["Microbiome of diseased and healthy implants\u2014a comprehensive microbial data analysis"],"prefix":"10.3389","volume":"14","author":[{"given":"Pingyi","family":"Jia","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinran","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jinchen","family":"Ye","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongye","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingwen","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianxia","family":"Hou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,8,29]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"332","DOI":"10.1099\/jmm.0.000682","article-title":"Shift of microbial composition of peri-implantitis-associated oral biofilm as revealed by 16S rRNA gene cloning","volume":"67","author":"Al-Ahmad","year":"2018","journal-title":"J. Med. Microbiol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1186\/s12967-022-03636-9","article-title":"Host-microbiome interactions regarding peri-implantitis and dental implant loss","volume":"20","author":"Alves","year":"2022","journal-title":"J. Transl. Med."},{"key":"B3","doi-asserted-by":"publisher","first-page":"2771","DOI":"10.1007\/s00784-021-04253-4","article-title":"Microbiome differences in periodontal, peri-implant, and healthy sites: a cross-sectional pilot study","volume":"26","author":"Barbagallo","year":"2022","journal-title":"Clin. Oral. Investig."},{"key":"B4","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1177\/0022034520949851","article-title":"Microbial community-driven etiopathogenesis of peri-implantitis","volume":"100","author":"Belibasakis","year":"2021","journal-title":"J. Dent. Res."},{"key":"B5","doi-asserted-by":"publisher","first-page":"S313","DOI":"10.1002\/JPER.17-0739","article-title":"Peri-implant diseases and conditions: Consensus report of workgroup 4 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions","author":"Berglundh","year":"2018","journal-title":"J. Periodontol"},{"key":"B6","first-page":"1","article-title":"Literacy and health outcomes","author":"Berkman","year":"2004","journal-title":"Evid Rep. Technol. Assess. (Summ)"},{"key":"B7","doi-asserted-by":"publisher","first-page":"S1","DOI":"10.1111\/jcpe.12935","article-title":"A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification","author":"Caton","year":"2018","journal-title":"J. Clin. Periodontol"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1093\/database\/baq013","article-title":"The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information","volume":"2010","author":"Chen","year":"2010","journal-title":"Database (Oxford)"},{"key":"B9","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1111\/prd.12447","article-title":"Risk factors for periodontitis & peri-implantitis","volume":"90","author":"Darby","year":"2022","journal-title":"Periodontol 2000"},{"key":"B10","doi-asserted-by":"publisher","first-page":"1192","DOI":"10.1111\/clr.12231","article-title":"Microbiological diversity of peri-implantitis biofilm by Sanger sequencing","volume":"25","author":"da Silva","year":"2014","journal-title":"Clin. Oral. Implants Res."},{"key":"B11","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1186\/s12903-022-02493-8","article-title":"What is the prevalence of peri-implantitis? A systematic review and meta-analysis","volume":"22","author":"Diaz","year":"2022","journal-title":"BMC Oral. Health"},{"key":"B12","doi-asserted-by":"publisher","first-page":"372","DOI":"10.1111\/cid.12457","article-title":"Long-term effect of surface roughness and patients\u2019 Factors on crestal bone loss at dental implants. A systematic review and meta-analysis","volume":"19","author":"Doornewaard","year":"2017","journal-title":"Clin. Implant Dent. Relat. Res."},{"key":"B13","doi-asserted-by":"publisher","first-page":"1297","DOI":"10.1902\/jop.2017.160808","article-title":"Smoking may lead to marginal bone loss around non-submerged implants during bone healing by altering salivary microbiome: A prospective study","volume":"88","author":"Duan","year":"2017","journal-title":"J. Periodontol"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1128\/mSystems.00187-18","article-title":"New insights into human nostril microbiome from the expanded human oral microbiome database (eHOMD): a resource for the microbiome of the human aerodigestive tract","volume":"3","author":"Escapa","year":"2018","journal-title":"mSystems"},{"key":"B15","doi-asserted-by":"publisher","first-page":"422","DOI":"10.1111\/j.1600-0722.1997.tb02139.x","article-title":"Transmission electron microscopic study of in vivo pellicle formation on dental restorative materials","volume":"105","author":"Hannig","year":"1997","journal-title":"Eur. J. Oral. Sci."},{"key":"B16","doi-asserted-by":"publisher","first-page":"5284","DOI":"10.1038\/s41598-022-09192-y","article-title":"Microbial differences between active and remission peri-implantitis","volume":"12","author":"Hashimoto","year":"2022","journal-title":"Sci. Rep."},{"key":"B17","doi-asserted-by":"publisher","first-page":"791","DOI":"10.1038\/s41415-024-7402-z","article-title":"Peri-implant mucositis and peri-implantitis: key features and differences","volume":"236","author":"Heitz-Mayfield","year":"2024","journal-title":"Br. Dent. J."},{"key":"B18","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1111\/clr.13307","article-title":"Group 4 ITI Consensus Report: Risks and biologic complications associated with implant dentistry","author":"Heitz-Mayfield","year":"2018","journal-title":"Clin. Oral. Implants Res."},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1016\/j.anaerobe.2021.102506","article-title":"First description of Lachnoanaerobaculum orale as a possible cause of human bacteremia","volume":"73","author":"Ida","year":"2022","journal-title":"Anaerobe"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1016\/j.micpath.2021.105100","article-title":"The temporal shift of peri-implant microbiota during the biofilm formation and maturation in a canine model","volume":"158","author":"Jiang","year":"2021","journal-title":"Microb. Pathog."},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2023.1121273","article-title":"The causality between intestinal flora and allergic diseases: Insights from a bi-directional two-sample Mendelian randomization analysis","volume":"14","author":"Jin","year":"2023","journal-title":"Front. Immunol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"5029","DOI":"10.1038\/s41467-019-13036-1","article-title":"Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis","volume":"10","author":"Johnson","year":"2019","journal-title":"Nat. Commun."},{"key":"B23","doi-asserted-by":"publisher","first-page":"210","DOI":"10.1111\/jopr.13270","article-title":"Microbiological profile and human immune response associated with peri-implantitis: A systematic review","volume":"30","author":"Kensara","year":"2021","journal-title":"J. Prosthodont"},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0218266","article-title":"Fretibacterium sp. human oral taxon 360 is a novel biomarker for periodontitis screening in the Japanese population","volume":"14","author":"Khemwong","year":"2019","journal-title":"PloS One"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2020.596490","article-title":"Discriminating microbial community structure between peri-implantitis and periodontitis with integrated metagenomic, metatranscriptomic, and network analysis","volume":"10","author":"Komatsu","year":"2020","journal-title":"Front. Cell Infect. Microbiol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1111\/prd.12372","article-title":"Peri-implantitis is not periodontitis: Scientific discoveries shed light on microbiome-biomaterial interactions that may determine disease phenotype","volume":"86","author":"Kotsakis","year":"2021","journal-title":"Periodontol 2000"},{"key":"B27","doi-asserted-by":"publisher","first-page":"2","DOI":"10.3402\/jom.v2i0.5104","article-title":"Analysis of microbiota associated with peri-implantitis using 16S rRNA gene clone library","volume":"24","author":"Koyanagi","year":"2010","journal-title":"J. Oral. Microbiol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1498","DOI":"10.1111\/jcpe.13023","article-title":"The severity of human peri-implantitis lesions correlates with the level of submucosal microbial dysbiosis","volume":"45","author":"Kroger","year":"2018","journal-title":"J. Clin. Periodontol"},{"key":"B29","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1111\/j.1600-051X.2012.01856.x","article-title":"Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants","volume":"39","author":"Kumar","year":"2012","journal-title":"J. Clin. Periodontol"},{"key":"B30","first-page":"568","article-title":"Study on microbial diversity of peri-implantitis subgingival by high-throughput sequencing","volume":"46","author":"Li","year":"2015","journal-title":"Sichuan Da Xue Bao Yi Xue Ban"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2023.1160993","article-title":"Causal effects of gut microbiota on the risk of periodontitis: a two-sample Mendelian randomization study","volume":"13","author":"Luo","year":"2023","journal-title":"Front. Cell Infect. Microbiol."},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1038\/srep06602","article-title":"Intraindividual variation in core microbiota in peri-implantitis and periodontitis","volume":"4","author":"Maruyama","year":"2014","journal-title":"Sci. Rep."},{"key":"B33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1034\/j.1600-0501.1990.010101.x","article-title":"Microbiological features of stable osseointegrated implants used as abutments for overdentures","volume":"1","author":"Mombelli","year":"1990","journal-title":"Clin. Oral. Implants Res."},{"key":"B34","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1111\/jre.12708","article-title":"Pyrosequencing of the subgingival microbiome in peri-implantitis after non-surgical mechanical debridement therapy","volume":"55","author":"Nie","year":"2020","journal-title":"J. Periodontal Res."},{"key":"B35","doi-asserted-by":"publisher","first-page":"10575","DOI":"10.1038\/s41598-023-37522-1","article-title":"Rapid and easy construction of a simplified amplicon sequencing (simplified AmpSeq) library for marker-assisted selection","volume":"13","author":"Nishio","year":"2023","journal-title":"Sci. Rep."},{"key":"B36","doi-asserted-by":"publisher","first-page":"711","DOI":"10.1177\/0022034516634619","article-title":"Levels of candidate periodontal pathogens in subgingival biofilm","volume":"95","author":"Oliveira","year":"2016","journal-title":"J. Dent. Res."},{"key":"B37","doi-asserted-by":"publisher","first-page":"961","DOI":"10.3390\/ijms25020961","article-title":"Correlation between inflammasomes and microbiota in peri-implantitis","volume":"25","author":"Padial-Molina","year":"2024","journal-title":"Int. J. Mol. Sci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1054\/modi.2001.29158","article-title":"16S rRNA gene sequencing for bacterial pathogen identification in the clinical laboratory","volume":"6","author":"Patel","year":"2001","journal-title":"Mol. Diagn."},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.2584","article-title":"VSEARCH: a versatile open source tool for metagenomics","volume":"4","author":"Rognes","year":"2016","journal-title":"PeerJ"},{"key":"B40","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1111\/clr.13787","article-title":"Evaluation of different materials used for sealing of implant abutment access channel and the peri-implant sulcus microbiota: A 6-month, randomized controlled trial","volume":"32","author":"Rubino","year":"2021","journal-title":"Clin. Oral. Implants Res."},{"key":"B41","doi-asserted-by":"publisher","DOI":"10.14309\/ctg.0000000000000569","article-title":"Dietary calcium and risk of microscopic colitis","volume":"14","author":"Sandler","year":"2023","journal-title":"Clin. Transl. Gastroenterol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1274","DOI":"10.1111\/jcpe.12788","article-title":"Exploring the microbiome of healthy and diseased peri-implant sites using Illumina sequencing","volume":"44","author":"Sanz-Martin","year":"2017","journal-title":"J. Clin. Periodontol"},{"key":"B43","doi-asserted-by":"publisher","first-page":"975","DOI":"10.1111\/j.1600-0501.2008.01566.x","article-title":"Composition of supra- and subgingival biofilm of subjects with healthy and diseased implants","volume":"19","author":"Shibli","year":"2008","journal-title":"Clin. Oral. Implants Res."},{"key":"B44","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1111\/j.1600-051x.1998.tb02419.x","article-title":"Microbial complexes in subgingival plaque","volume":"25","author":"Socransky","year":"1998","journal-title":"J. Clin. Periodontol"},{"key":"B45","doi-asserted-by":"publisher","first-page":"30","DOI":"10.19723\/j.issn.1671-167X.2023.01.005","article-title":"Profiles and differences of submucosal microbial in peri-implantitis and health implants: A cross-sectional study","volume":"55","author":"Sun","year":"2023","journal-title":"Beijing Da Xue Bao Yi Xue Ban"},{"key":"B46","doi-asserted-by":"publisher","first-page":"6703","DOI":"10.7150\/thno.57775","article-title":"Machine learning-assisted immune profiling stratifies peri-implantitis patients with unique microbial colonization and clinical outcomes","volume":"11","author":"Wang","year":"2021","journal-title":"Theranostics"},{"key":"B47","unstructured":"The Newcastle-Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses\n          \n          \n            \n              Wells\n              G. A.\n            \n            \n              Shea\n              B.\n            \n            \n              O\u2019Connell\n              D.\n            \n            \n              Peterson\n              J.\n            \n            \n              Welch\n              V.\n            \n            \n              Losos\n              M.\n            \n          \n          \n          2009"},{"key":"B48","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1038\/s41368-018-0018-x","article-title":"The oral microbiome bank of China","volume":"10","author":"Xian","year":"2018","journal-title":"Int. J. Oral. Sci."},{"key":"B49","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1038\/nrmicro3330","article-title":"Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences","volume":"12","author":"Yarza","year":"2014","journal-title":"Nat. Rev. Microbiol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"760","DOI":"10.1111\/clr.13459","article-title":"Intra-oral single-site comparisons of periodontal and peri-implant microbiota in health and disease","volume":"30","author":"Yu","year":"2019","journal-title":"Clin. Oral. Implants Res."},{"key":"B51","doi-asserted-by":"publisher","first-page":"2936","DOI":"10.1038\/s41396-020-0720-5","article-title":"Predicting disease occurrence with high accuracy based on soil macroecological patterns of Fusarium wilt","volume":"14","author":"Yuan","year":"2020","journal-title":"ISME J."},{"key":"B52","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2019.00476","article-title":"The oral microbiota may have influence on oral cancer","volume":"9","author":"Zhang","year":"2019","journal-title":"Front. Cell Infect. Microbiol."},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1038\/srep10948","article-title":"Subgingival microbiome in patients with healthy and ailing dental implants","volume":"5","author":"Zheng","year":"2015","journal-title":"Sci. Rep."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2024.1445751\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,29]],"date-time":"2024-08-29T05:10:22Z","timestamp":1724908222000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2024.1445751\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8,29]]},"references-count":53,"alternative-id":["10.3389\/fcimb.2024.1445751"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2024.1445751","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,8,29]]},"article-number":"1445751"}}