Exploring the Microbiome of Healthy and Diseased Peri-implant Sites Using Illumina Sequencing

Overview

Journal J Clin Periodontol

Date 2017 Aug 3

PMID 28766745

Citations 65

Authors

Ignacio Sanz-Martin

Janet Doolittle-Hall

Ricardo P Teles

Michele Patel

Georgios N Belibasakis

Christoph H F Hammerle

Ronald E Jung

Flavia R F Teles

Affiliations

Soon will be listed here.

Abstract

Aim: To compare the microbiome of healthy (H) and diseased (P) peri-implant sites and determine the core peri-implant microbiome.

Materials And Methods: Submucosal biofilms from 32 H and 35 P sites were analysed using 16S rRNA sequencing (MiSeq, Illumina), QIIME and HOMINGS. Differences between groups were determined using principal coordinate analysis (PCoA), t tests and Wilcoxon rank sum test and FDR-adjusted. The peri-implant core microbiome was determined.

Results: PCoA showed partitioning between H and P at all taxonomic levels. Bacteroidetes, Spirochetes and Synergistetes were higher in P, while Actinobacteria prevailed in H (p < .05). Porphyromonas and Treponema were more abundant in P while Rothia and Neisseria were higher in H (p < .05). The core peri-implant microbiome contained Fusobacterium, Parvimonas and Campylobacter sp. T. denticola, and P. gingivalis levels were higher in P, as well as F. alocis, F. fastidiosum and T. maltophilum (p < .05).

Conclusion: The peri-implantitis microbiome is commensal-depleted and pathogen-enriched, harbouring traditional and new pathogens. The core peri-implant microbiome harbours taxa from genera often associated with periodontal inflammation.

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References

Hajishengallis G, Lambris J . Complement and dysbiosis in periodontal disease. Immunobiology. 2012; 217(11):1111-6. PMC: 3439646. DOI: 10.1016/j.imbio.2012.07.007. View

Carcuac O, Derks J, Charalampakis G, Abrahamsson I, Wennstrom J, Berglundh T . Adjunctive Systemic and Local Antimicrobial Therapy in the Surgical Treatment of Peri-implantitis: A Randomized Controlled Clinical Trial. J Dent Res. 2015; 95(1):50-7. DOI: 10.1177/0022034515601961. View

Charalampakis G, Belibasakis G . Microbiome of peri-implant infections: lessons from conventional, molecular and metagenomic analyses. Virulence. 2015; 6(3):183-7. PMC: 4601299. DOI: 10.4161/21505594.2014.980661. View

Abusleme L, Dupuy A, Dutzan N, Silva N, Burleson J, Strausbaugh L . The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J. 2013; 7(5):1016-25. PMC: 3635234. DOI: 10.1038/ismej.2012.174. View

Heitz-Mayfield L . Peri-implant diseases: diagnosis and risk indicators. J Clin Periodontol. 2008; 35(8 Suppl):292-304. DOI: 10.1111/j.1600-051X.2008.01275.x. View

Baker G, Smith J, Cowan D . Review and re-analysis of domain-specific 16S primers. J Microbiol Methods. 2003; 55(3):541-55. DOI: 10.1016/j.mimet.2003.08.009. View

Shibli J, Melo L, Ferrari D, Figueiredo L, Faveri M, Feres M . Composition of supra- and subgingival biofilm of subjects with healthy and diseased implants. Clin Oral Implants Res. 2008; 19(10):975-82. DOI: 10.1111/j.1600-0501.2008.01566.x. View

Maruyama N, Maruyama F, Takeuchi Y, Aikawa C, Izumi Y, Nakagawa I . Intraindividual variation in core microbiota in peri-implantitis and periodontitis. Sci Rep. 2014; 4:6602. PMC: 4194447. DOI: 10.1038/srep06602. View

. Structure, function and diversity of the healthy human microbiome. Nature. 2012; 486(7402):207-14. PMC: 3564958. DOI: 10.1038/nature11234. View

10.

Zitzmann N, Berglundh T . Definition and prevalence of peri-implant diseases. J Clin Periodontol. 2008; 35(8 Suppl):286-91. DOI: 10.1111/j.1600-051X.2008.01274.x. View

11.

Belstrom D, Holmstrup P, Fiehn N, Kirkby N, Kokaras A, Paster B . Salivary microbiota in individuals with different levels of caries experience. J Oral Microbiol. 2017; 9(1):1270614. PMC: 5328370. DOI: 10.1080/20002297.2016.1270614. View

12.

McIntyre M, Peacock T, Akers K, Burmeister D . Initial Characterization of the Pig Skin Bacteriome and Its Effect on In Vitro Models of Wound Healing. PLoS One. 2016; 11(11):e0166176. PMC: 5100914. DOI: 10.1371/journal.pone.0166176. View

13.

Deng Z, Szafranski S, Jarek M, Bhuju S, Wagner-Dobler I . Dysbiosis in chronic periodontitis: Key microbial players and interactions with the human host. Sci Rep. 2017; 7(1):3703. PMC: 5473847. DOI: 10.1038/s41598-017-03804-8. View

14.

Amarasekara R, Jayasekara R, Senanayake H, Dissanayake V . Microbiome of the placenta in pre-eclampsia supports the role of bacteria in the multifactorial cause of pre-eclampsia. J Obstet Gynaecol Res. 2014; 41(5):662-9. DOI: 10.1111/jog.12619. View

15.

Gomes B, Berber V, Kokaras A, Chen T, Paster B . Microbiomes of Endodontic-Periodontal Lesions before and after Chemomechanical Preparation. J Endod. 2015; 41(12):1975-84. PMC: 7061340. DOI: 10.1016/j.joen.2015.08.022. View

16.

Ma N, Yang D, Okamura H, Teramachi J, Hasegawa T, Qiu L . Involvement of interleukin‑23 induced by Porphyromonas endodontalis lipopolysaccharide in osteoclastogenesis. Mol Med Rep. 2016; 15(2):559-566. PMC: 5364876. DOI: 10.3892/mmr.2016.6041. View

17.

Backhed F, Fraser C, Ringel Y, Sanders M, Sartor R, Sherman P . Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe. 2012; 12(5):611-22. DOI: 10.1016/j.chom.2012.10.012. View

18.

Derks J, Tomasi C . Peri-implant health and disease. A systematic review of current epidemiology. J Clin Periodontol. 2014; 42 Suppl 16:S158-71. DOI: 10.1111/jcpe.12334. View

19.

Derks J, Schaller D, Hakansson J, Wennstrom J, Tomasi C, Berglundh T . Peri-implantitis - onset and pattern of progression. J Clin Periodontol. 2016; 43(4):383-8. DOI: 10.1111/jcpe.12535. View

20.

Pei A, Oberdorf W, Nossa C, Agarwal A, Chokshi P, Gerz E . Diversity of 16S rRNA genes within individual prokaryotic genomes. Appl Environ Microbiol. 2010; 76(12):3886-97. PMC: 2893482. DOI: 10.1128/AEM.02953-09. View