Community dynamics during de novo colonization of the nascent peri-implant sulcus
Tamires Pereira Dutra , Nicolas Robitaille , Khaled Altabtbaei , Shareef M. Dabdoub , Purnima S. Kumar
International Journal of Oral Science ›› 2025, Vol. 17 ›› Issue (1) : 37
Community dynamics during de novo colonization of the nascent peri-implant sulcus
Dental implants have restored masticatory function to over 100 000 000 individuals, yet almost 1 000 000 implants fail each year due to peri-implantitis, a disease triggered by peri-implant microbial dysbiosis. Our ability to prevent and treat peri-implantitis is hampered by a paucity of knowledge of how these biomes are acquired and the factors that engender normobiosis. Therefore, we combined a 3-month interventional study of 15 systemically and periodontally healthy adults with whole genome sequencing, fine-scale enumeration and graph theoretics to interrogate colonization dynamics in the pristine peri-implant sulcus. We discovered that colonization trajectories of implants differ substantially from adjoining teeth in acquisition of new members and development of functional synergies. Source-tracking algorithms revealed that this niche is initially seeded by bacteria trapped within the coverscrew chamber during implant placement. These pioneer species stably colonize the microbiome and exert a sustained influence on the ecosystem by serving as anchors of influential hubs and by providing functions that enable cell replication and biofilm maturation. Unlike the periodontal microbiome, recruitment of new members to the peri-implant community occurs on nepotistic principles. Maturation is accompanied by a progressive increase in anaerobiosis, however, the predominant functionalities are oxygen-dependent over the 12-weeks. The peri-implant community is easily perturbed following crown placement, but demonstrates remarkable resilience; returning to pre-perturbation states within three weeks. This study highlights important differences in the development of the periodontal and peri-implant ecosystems, and signposts the importance of placing implants in periodontally healthy individuals or following the successful resolution of periodontal disease.
| [1] |
NIDCR. Tooth Loss Among Adults 20−64. http://www.nidcr.nih.gov/DataStatistics/FindDataByTopic/ToothLoss/ToothLossAdults20to64.htm (2014). |
| [2] |
Emami, E., De Souza, R. F., Kabawat M. & Feine J. S. The impact of edentulism on oral and general health. Int. J. Dentistry. 2013, 1−7 (2013). |
| [3] |
Jain, N., Dutt, U., Radenkov, I. & Jain S. WHO’s global oral health status report 2022: Actions, discussion and implementation. Oral Dis. 30, 73–79 (2023). |
| [4] |
|
| [5] |
|
| [6] |
|
| [7] |
|
| [8] |
|
| [9] |
|
| [10] |
Belibasakis, G. N. & Manoil, D. Microbial community-driven etiopathogenesis of peri-implantitis. J. Dental Res. 100, 21–28 (2021). |
| [11] |
|
| [12] |
Dabdoub, S. M., Tsigarida, A. A. & Kumar P. S. Patient-specific analysis of periodontal and peri-implant microbiomes. J. Dent. Res.92, 168S–75S (2013). |
| [13] |
Sinjab, K. et al. Impact of surface characteristics on the peri-implant microbiome in health and disease. J. Periodontol.95, 244−255 (2024). |
| [14] |
|
| [15] |
Quirynen, M. et al. Initial subgingival colonization of ‘pristine’ pockets. 2005. |
| [16] |
Payne, J. B. et al. Subgingival microbiome colonization and cytokine production during early dental implant healing. mSphere. 2, e00527−17 (2017). |
| [17] |
|
| [18] |
|
| [19] |
|
| [20] |
Silva-Boghossian, C. M., Duarte, P. T., Silva DG, da, Lourenço, T. G. B. & Colombo, A. P. V. Colonization dynamics of subgingival microbiota in recently installed dental implants compared to healthy teeth in the same individual: a 6-month prospective observational study. J. Appl. Oral Sci. 31, 1−10 (2023). |
| [21] |
Avila, M., Ojcius, D. M. & Zlem, Y. Ö. The oral microbiota: living with a permanent guest. DNA Cell Biol. 28, 405–411 (2009). |
| [22] |
De Wit, R. & Bouvier, T. ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ. Microbiol. 8, 755–758 (2006). |
| [23] |
Holmberg, T. J. BIOL 1213. LibreTexts; Northwestern Connecticut Community College https://bio.libretexts.org/@go/page/79240 (2022). Retrieved from https://bio.libretexts.org/Sandboxes/tholmberg_at_nwcc.edu/BIOL_1213 |
| [24] |
Clark, M. A., Douglas, M. & Choi, J. Biology 2e. 2nd edn. Vol. 1. (OpenStax; 2018). |
| [25] |
Sottosanti, K. ‘pioneer species’. In: Encyclopedia Britannica. https://www.britannica.com/science/pioneer-species (2023). |
| [26] |
Darwin, C. On the Origin of Species (Murray, 1859). |
| [27] |
|
| [28] |
Sumida, S., Kazuyuki, I., Kishi, M. & Okuda, K. Transmission of periodontal disease-associated bacteria from teeth to osseointegrated implant Regions. 17, 696–702 (2002). |
| [29] |
|
| [30] |
Connell, J. H. & Slatyer, R. O. Mechanisms of succession in natural communities and their role in community stability and organization. American Naturalist. 111, 1119−1144 (1977). |
| [31] |
|
| [32] |
|
| [33] |
|
| [34] |
|
| [35] |
|
| [36] |
|
| [37] |
Duran-Pinedo, A. et al. Long-term dynamics of the human oral microbiome during clinical disease progression. BMC Biol. 19, 2−17 (2021). |
| [38] |
|
| [39] |
|
| [40] |
|
| [41] |
Escapa, I. F. et al. New Insights into Human Nostril Microbiome from the Expanded Human Oral Microbiome Database (eHOMD): a Resource for the Microbiome of the Human Aerodigestive Tract. mSystems. 3, 1−20 (2018). |
| [42] |
|
| [43] |
|
| [44] |
|
| [45] |
Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019). |
| [46] |
Dabdoub, S. M. et al. PhyloToAST: Bioinformatics tools for species-level analysis and visualization of complex microbial datasets. Sci. Rep. 6, 1−9 (2016). |
| [47] |
|
| [48] |
Han, R., Shi, P. & Zhang, A. R. Guaranteed functional tensor singular value decomposition. J. Am. Stat. Assoc.119, 995–1007 (2023). |
| [49] |
Shi, P., Martino, C., Han, R. et al. TEMPTED: time-informed dimensionality reduction for longitudinal microbiome studies. Genome. Biol. 25, 317 (2024). |
| [50] |
McGhee, J. J. et al. Meta-SourceTracker: Application of Bayesian source tracking to shotgun metagenomics. PeerJ. 8, 2−18 (2020). |
| [51] |
|
| [52] |
Bastian, M., Heymann, S., & Jacomy, M. (2009). Gephi: an open source software for exploring and manipulating networks. In Proc. International AAAI Conference on Web and Social Media, 3(1), 361−362. https://doi.org/10.1609/icwsm.v3i1.13937. |
| [53] |
Xia, L. C. et al. Extended local similarity analysis (eLSA) of microbial community and other time series data with replicates. BMC Syst. Biol. 5, 1−12 (2011). |
| [54] |
|
The Author(s)
/
| 〈 |
|
〉 |