Mucosal bleeding correlates with submucosal microbial dysbiosis in peri-implant mucositis of patients with periodontitis.
microbial dysbiosis index
microbiome
modified sulcus bleeding index
peri-implant mucositis
Journal
Clinical oral implants research
ISSN: 1600-0501
Titre abrégé: Clin Oral Implants Res
Pays: Denmark
ID NLM: 9105713
Informations de publication
Date de publication:
Sep 2023
Sep 2023
Historique:
revised:
05
06
2023
received:
11
12
2022
accepted:
11
06
2023
medline:
6
9
2023
pubmed:
26
6
2023
entrez:
26
6
2023
Statut:
ppublish
Résumé
This study aimed to investigate the relationship between microbial communities and the severity of peri-implant mucosal bleeding in peri-implant mucositis. Submucosal plaque samples were collected from 54 implants divided into the healthy implant (HI) group, peri-implant mucositis (PM) group, and peri-implantitis (PI) group. Sequencing of 16S rRNA was performed using the Illumina MiSeq platform. Alpha diversity (i.e., Shannon and Chao index) and beta diversity were used to measure microbial diversity within and between microbial communities, respectively. Differences in microbial taxa between groups were assessed via linear discriminate analysis effect size. Correlation between the modified sulcus bleeding index (mSBI) and microbial dysbiosis index (MDI) was examined using Spearman correlation analysis and linear models. The submucosal bacterial richness (Chao index) was positively correlated with the mean mSBI in the PM group. As the mean mSBI increased in the PM group, the beta diversity became closer to that of the PI group. In the PM group, the abundances of 47 genera were significantly correlated with the mean mSBI, and the MDI was positively associated with the mean mSBI. Fourteen of the forty-seven genera were discriminative taxa between the HI and PI groups, and the abundances of these biomarkers became closer to those in the PI group in the progression of peri-implant disease. A higher mSBI value corresponded to a higher risk of microbial dysbiosis in peri-implant mucositis. The biomarkers identified may be useful for monitoring the progression of peri-implant disease.
Substances chimiques
Dental Implants
0
RNA, Ribosomal, 16S
0
Biomarkers
0
Types de publication
Journal Article
Langues
eng
Pagination
947-957Subventions
Organisme : National Natural Science Foundation of China
ID : 82173647
Organisme : Peking University Clinical Scientist Program
ID : BMU2019LCKXJ010
Informations de copyright
© 2023 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Abrahamsson, K. H., Wennström, J. L., Berglundh, T., & Abrahamsson, I. (2017). Altered expectations on dental implant therapy; views of patients referred for treatment of peri-implantitis. Clinical Oral Implants Research, 28(4), 437-442. https://doi.org/10.1111/clr.12817
Al-Ahmad, A., Muzafferiy, F., Anderson, A. C., Wolber, J. P., Ratka-Kruger, P., Fretwurst, T., Nelson, K., Vach, K., & Hellwig, E. (2018). Shift of microbial composition of peri-implantitis-associated oral biofilm as revealed by 16S rRNA gene cloning. Journal of Medical Microbiology, 67(3), 332-340. https://doi.org/10.1099/jmm.0.000682
Apatzidou, D., Lappin, D. F., Hamilton, G., Papadopoulos, C. A., Konstantinidis, A., & Riggio, M. P. (2017). Microbiome of peri-implantitis affected and healthy dental sites in patients with a history of chronic periodontitis. Archives of Oral Biology, 83, 145-152. https://doi.org/10.1016/j.archoralbio.2017.07.007
Arikan, M., Yildiz, Z., Demir, T. K., Yilmaz, N. H., Sen, A., Hanoglu, L., & Yildirim, S. (2022). Axillary microbiota is associated with cognitive impairment in Parkinson's disease patients. Microbiology Spectrum, 10(1), e0235821. https://doi.org/10.1128/spectrum.02358-21
Atsuta, I., Ayukawa, Y., Kondo, R., Oshiro, W., Matsuura, Y., Furuhashi, A., Tsukiyama, Y., & Koyano, K. (2016). Soft tissue sealing around dental implants based on histological interpretation. Journal of Prosthodontic Research, 60(1), 3-11. https://doi.org/10.1016/j.jpor.2015.07.001
Barbagallo, G., Santagati, M., Guni, A., Torrisi, P., Spitale, A., Stefani, S., Ferlito, S., & Nibali, L. (2021). Microbiome differences in periodontal, peri-implant, and healthy sites: A cross-sectional pilot study. Clinical Oral Investigations, 26(3), 2771-2781. https://doi.org/10.1007/s00784-021-04253-4
Belibasakis, G. N., & Manoil, D. (2020). Microbial community-driven etiopathogenesis of peri-implantitis. Journal of Dental Research, 100(1), 21-28. https://doi.org/10.1177/0022034520949851
Berglundh, T., Armitage, G., Araujo, M. G., Avila-Ortiz, G., Blanco, J., Camargo, P. M., Chen, S., Cochran, D., Derks, J., Figuero, E., Hämmerle, C. H. F., Heitz-Mayfield, L. J. A., Huynh-Ba, G., Iacono, V., Koo, K. T., Lambert, F., McCauley, L., Quirynen, M., Renvert, S., … Zitzmann, N. (2018). 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. Journal of Periodontology, 89(Suppl 1), S313-S318. https://doi.org/10.1002/jper.17-0739
Bolyen, E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C. C., Al-Ghalith, G. A., Alexander, H., Alm, E. J., Arumugam, M., Asnicar, F., Bai, Y., Bisanz, J. E., Bittinger, K., Brejnrod, A., Brislawn, C. J., Brown, C. T., Callahan, B. J., Caraballo-Rodríguez, A. M., Chase, J., … Caporaso, J. G. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37(8), 852-857. https://doi.org/10.1038/s41587-019-0209-9
Buser, D., Sennerby, L., & De Bruyn, H. (2017). Modern implant dentistry based on osseointegration: 50 years of progress, current trends and open questions. Periodontology 2000, 73(1), 7-21. https://doi.org/10.1111/prd.12185
Callahan, B. J., McMurdie, P. J., & Holmes, S. P. (2017). Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. The ISME Journal, 11(12), 2639-2643. https://doi.org/10.1038/ismej.2017.119
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581-583. https://doi.org/10.1038/nmeth.3869
Camelo-Castillo, A., Novoa, L., Balsa-Castro, C., Blanco, J., Mira, A., & Tomás, I. (2015). Relationship between periodontitis-associated subgingival microbiota and clinical inflammation by 16S pyrosequencing. Journal of Clinical Periodontology, 42(12), 1074-1082. https://doi.org/10.1111/jcpe.12470
Carcuac, O., Abrahamsson, I., Albouy, J. P., Linder, E., Larsson, L., & Berglundh, T. (2013). Experimental periodontitis and peri-implantitis in dogs. Clinical Oral Implants Research, 24(4), 363-371. https://doi.org/10.1111/clr.12067
Caton, J. G., Armitage, G., Berglundh, T., Chapple, I. L. C., Jepsen, S., Kornman, K. S., Mealey, B. L., Papapanou, P. N., Sanz, M., & Tonetti, M. S. (2018). A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. Journal of Clinical Periodontology, 45, S1-S8. https://doi.org/10.1111/jcpe.12935
Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11, 265-270.
de Melo, F., Milanesi, F. C., Angst, P. D. M., & Oppermann, R. V. (2020). A systematic review of the microbiota composition in various peri-implant conditions: Data from 16S rRNA gene sequencing. Archives of Oral Biology, 117, 104776. https://doi.org/10.1016/j.archoralbio.2020.104776
Gao, X., Zhou, J., Sun, X., Li, X., & Zhou, Y. (2018). Diversity analysis of subgingival microbial bacteria in peri-implantitis in Uygur population. Medicine (Baltimore), 97(5), e9774. https://doi.org/10.1097/md.0000000000009774
Gevers, D., Kugathasan, S., Denson, L. A., Vazquez-Baeza, Y., Van Treuren, W., Ren, B., Schwager, E., Knights, D., Song, S. J., Yassour, M., Morgan, X. C., Kostic, A. D., Luo, C., González, A., McDonald, D., Haberman, Y., Walters, T., Baker, S., Rosh, J., … Xavier, R. J. (2014). The treatment-naive microbiome in new-onset Crohn's disease. Cell Host & Microbe, 15(3), 382-392. https://doi.org/10.1016/j.chom.2014.02.005
Ghensi, P., Manghi, P., Zolfo, M., Armanini, F., Pasolli, E., Bolzan, M., Bertelle, A., Dell'Acqua, F., Dellasega, E., Waldner, R., Tessarolo, F., Tomasi, C., & Segata, N. (2020). Strong oral plaque microbiome signatures for dental implant diseases identified by strain-resolution metagenomics. NPJ Biofilms Microbiomes, 6(1), 47. https://doi.org/10.1038/s41522-020-00155-7
Karlsson, K., Derks, J., Wennström, J. L., Petzold, M., & Berglundh, T. (2020). Occurrence and clustering of complications in implant dentistry. Clinical Oral Implants Research, 31(10), 1002-1009. https://doi.org/10.1111/clr.13647
Korsch, M., Marten, S. M., Stoll, D., Prechtl, C., & Dötsch, A. (2021). Microbiological findings in early and late implant loss: An observational clinical case-controlled study. BMC Oral Health, 21(1), 112. https://doi.org/10.1186/s12903-021-01439-w
Kröger, A., Hülsmann, C., Fickl, S., Spinell, T., Hüttig, F., Kaufmann, F., Heimbach, A., Hoffmann, P., Enkling, N., Renvert, S., Schwarz, F., Demmer, R. T., Papapanou, P. N., Jepsen, S., & Kebschull, M. (2018). The severity of human peri-implantitis lesions correlates with the level of submucosal microbial dysbiosis. Journal of Clinical Periodontology, 45(12), 1498-1509. https://doi.org/10.1111/jcpe.13023
Kumar, P. S., Mason, M. R., Brooker, M. R., & O'Brien, K. (2012). Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. Journal of Clinical Periodontology, 39(5), 425-433. https://doi.org/10.1111/j.1600-051X.2012.01856.x
Lu, H., Zou, P., Zhang, Y., Zhang, Q., Chen, Z., & Chen, F. (2022). The sampling strategy of oral microbiome. iMeta, 1(2), e23. https://doi.org/10.1002/imt2.23
Lundmark, A., Hu, Y. O. O., Huss, M., Johannsen, G., Andersson, A. F., & Yucel-Lindberg, T. (2019). Identification of salivary microbiota and its association with host inflammatory mediators in periodontitis. Frontiers in Cellular and Infection Microbiology, 9, 216. https://doi.org/10.3389/fcimb.2019.00216
Marcantonio Junior, E., Romito, G. A., & Shibli, J. A. (2019). Peri-implantitis as a “burden” disease. Brazilian Oral Research, 33(suppl 1), e087. https://doi.org/10.1590/1807-3107bor-2019.vol33.0087
Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.Journal, 17(1), 10-12. https://doi.org/10.14806/ej.17.1.200
Mombelli, A., Van Oosten, M. A., Schurch, E., & Land, N. P. (1987). The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiology and Immunology, 2(4), 145-151. https://doi.org/10.1111/j.1399-302x.1987.tb00298.x
Newbrun, E. (1996). Indices to measure gingival bleeding. Journal of Periodontology, 67(6), 555-561. https://doi.org/10.1902/jop.1996.67.6.555
Nie, J., Zhang, Q., Zheng, H., Xu, L. X., Wang, X. Y., & Chen, F. (2020). Pyrosequencing of the subgingival microbiome in peri-implantitis after non-surgical mechanical debridement therapy. Journal of Periodontal Research, 55(2), 238-246. https://doi.org/10.1111/jre.12708
Polymeri, A., van der Horst, J., Buijs, M. J., Zaura, E., Wismeijer, D., Crielaard, W., Loos, B. G., Laine, M. L., & Brandt, B. W. (2021). Submucosal microbiome of peri-implant sites: A cross-sectional study. Journal of Clinical Periodontology, 48(9), 1228-1239. https://doi.org/10.1111/jcpe.13502
Salvi, G. E., Aglietta, M., Eick, S., Sculean, A., Lang, N. P., & Ramseier, C. A. (2012). Reversibility of experimental peri-implant mucositis compared with experimental gingivitis in humans. Clinical Oral Implants Research, 23(2), 182-190. https://doi.org/10.1111/j.1600-0501.2011.02220.x
Sanz-Martin, I., Doolittle-Hall, J., Teles, R. P., Patel, M., Belibasakis, G. N., Hämmerle, C. H. F., Jung, R. E., & Teles, F. R. F. (2017). Exploring the microbiome of healthy and diseased peri-implant sites using Illumina sequencing. Journal of Clinical Periodontology, 44(12), 1274-1284. https://doi.org/10.1111/jcpe.12788
Schwarz, F., Derks, J., Monje, A., & Wang, H. L. (2018). Peri-implantitis. Journal of Clinical Periodontology, 45(Suppl 20), S246-S266. https://doi.org/10.1111/jcpe.12954
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., & Huttenhower, C. (2011). Metagenomic biomarker discovery and explanation. Genome Biology, 12(6), R60. https://doi.org/10.1186/gb-2011-12-6-r60
Shannon, C. E. (1997). The mathematical theory of communication. 1963. MD Computing, 14(4), 306-317.
Shi, M., Wei, Y., Hu, W., Nie, Y., Wu, X., & Lu, R. (2018). The subgingival microbiome of periodontal pockets with different probing depths in chronic and aggressive periodontitis: A pilot study. Frontiers in Cellular and Infection Microbiology, 8, 124. https://doi.org/10.3389/fcimb.2018.00124
Shi, Y., Tong, Z., Zhang, Y., Si, M., & He, F. (2022). Microbial profiles of peri-implant mucositis and peri-implantitis: Submucosal microbial dysbiosis correlates with disease severity. Clinical Oral Implants Research, 33(2), 172-183. https://doi.org/10.1111/clr.13880
Shiba, T., Watanabe, T., Komatsu, K., Koyanagi, T., Nemoto, T., Ohsugi, Y., Michi, Y., Katagiri, S., Takeuchi, Y., Ishihara, K., & Iwata, T. (2021). Non-surgical treatment for periodontitis and peri-implantitis: Longitudinal clinical and bacteriological findings-a case report with a 7-year follow-up evaluation. SAGE Open Medical Case Reports, 9. https://doi.org/10.1177/2050313X211029154
Shimchuk, A. A., Weinstein, B. F., & Daubert, D. M. (2021). The impact of a change in classification criteria on the prevalence of peri-implantitis: A cross-sectional analysis. Journal of Periodontology, 92(9), 1339-1346. https://doi.org/10.1002/jper.20-0566
Sousa, V., Nibali, L., Spratt, D., Dopico, J., Mardas, N., Petrie, A., & Donos, N. (2017). Peri-implant and periodontal microbiome diversity in aggressive periodontitis patients: A pilot study. Clinical Oral Implants Research, 28(5), 558-570. https://doi.org/10.1111/clr.12834
Sun, F., Wei, Y., Li, S., Nie, Y., Wang, C., & Hu, W. (2022). Shift in the submucosal microbiome of diseased peri-implant sites after non-surgical mechanical debridement treatment. Frontiers in Cellular and Infection Microbiology, 12, 1091938. https://doi.org/10.3389/fcimb.2022.1091938
Tong, Y., Zheng, L., Qing, P., Zhao, H., Li, Y., Su, L., Zhang, Q., Zhao, Y., Luo, Y., & Liu, Y. (2020). Oral microbiota perturbations are linked to high risk for rheumatoid arthritis. Frontiers in Cellular and Infection Microbiology, 9, 475. https://doi.org/10.3389/fcimb.2019.00475
Tsigarida, A., Chochlidakis, K., Fraser, D., Lampraki, E., Einarsdottir, E. R., Barmak, A. B., Papaspyridakos, P., & Ercoli, C. (2020). Peri-implant diseases and biologic complications at implant-supported fixed dental prostheses in partially edentulous patients. Journal of Prosthodontics, 29(5), 429-435. https://doi.org/10.1111/jopr.13165
Tsigarida, A. A., Dabdoub, S. M., Nagaraja, H. N., & Kumar, P. S. (2015). The influence of smoking on the peri-implant microbiome. Journal of Dental Research, 94(9), 1202-1217. https://doi.org/10.1177/0022034515590581
van der Horst, J., Buijs, M. J., Laine, M. L., Wismeijer, D., Loos, B. G., Crielaard, W., & Zaura, E. (2013). Sterile paper points as a bacterial DNA-contamination source in microbiome profiles of clinical samples. Journal of Dentistry, 41(12), 1297-1301. https://doi.org/10.1016/j.jdent.2013.10.008
Wang, Q., Lu, H., Zhang, L., Yan, X., Zhu, B., & Meng, H. (2020). Peri-implant mucositis sites with suppuration have higher microbial risk than sites without suppuration. Journal of Periodontology, 91(10), 1284-1294. https://doi.org/10.1002/JPER.19-0634
Yan, Z., Yang, F., Cao, J., Ding, W., Yan, S., Shi, W., Wen, S., & Yao, L. (2021). Alterations of gut microbiota and metabolome with Parkinson's disease. Microbial Pathogenesis, 160, 105187. https://doi.org/10.1016/j.micpath.2021.105187
Yilmaz, P., Parfrey, L. W., Yarza, P., Gerken, J., Pruesse, E., Quast, C., Schweer, T., Peplies, J., Ludwig, W., & Glöckner, F. O. (2014). The SILVA and “all-species living tree project (LTP)” taxonomic frameworks. Nucleic Acids Research, 42(D1), D643-D648. https://doi.org/10.1093/nar/gkt1209
Yu, X. L., Chan, Y., Zhuang, L., Lai, H. C., Lang, N. P., Leung, W. K., & Watt, R. M. (2019). Intra-oral single-site comparisons of periodontal and peri-implant microbiota in health and disease. Clinical Oral Implants Research, 30(8), 760-776. https://doi.org/10.1111/clr.13459
Zheng, H., Xu, L., Wang, Z., Li, L., Zhang, J., Zhang, Q., Chen, T., Lin, J., & Chen, F. (2015). Subgingival microbiome in patients with healthy and ailing dental implants. Scientific Reports, 5, 10948. https://doi.org/10.1038/srep10948
Zitzmann, N. U., Berglundh, T., Marinello, C. P., & Lindhe, J. (2001). Experimental peri-implant mucositis in man. Journal of Clinical Periodontology, 28(6), 517-523. https://doi.org/10.1034/j.1600-051x.2001.028006517.x