Email Alert | RSS

Journal of Peking University (Health Sciences) ›› 2023, Vol. 55 ›› Issue (1): 30-37. doi: 10.19723/j.issn.1671-167X.2023.01.005

Previous Articles     Next Articles

Profiles and differences of submucosal microbial in peri-implantitis and health implants: A cross-sectional study

Fei SUN,Jian LIU,Si-qi LI,Yi-ping WEI,Wen-jie HU*(),Cui WANG*()   

  1. Department of Periodontology, Peking University School and Hospital of Stomatology & National Center of Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Research Center of Oral Biomaterials and Digital Medical Devices, Beijing 100081, China
  • Received:2022-10-10 Online:2023-02-18 Published:2023-01-31
  • Contact: Wen-jie HU,Cui WANG E-mail:huwenjie@pkuss.bjmu.edu.cn;wangcui881005@163.com
  • Supported by:
    the Beijing Natural Science Foundation(7214273);the National Natural Science Foundation of China(82173647);the Peking University Clinical Scientist Program(BMU2019LCKXJ010)

RICH HTML

   

PDF (PC)

Abstract:

Objective: To describe the submucosal microbial profiles of peri-implantitis and healthy implants, and to explore bacteria that might be correlated with clinical parameters. Methods: In the present cross-sectional study, 49 patients were recruited. Each patient contributed with one implant, submucosal biofilms were collected from 20 healthy implants and 29 implants with peri-implantitis. DNA was extracted and bacterial 16S ribosomal RNA (16S rRNA) genes were amplified. Submucosal biofilms were analyzed using 16S rRNA sequencing at Illumina MiSeq platform. Differences between the groups were determined by analyzing α diversity, microbial component and microbial structure. The potential correlation between the bacteria with pocket probing depth (PPD) of peri-implant calculated by Spearman correlation analysis. Results: The α diversity of submucosal microbial of health group was significantly lower than that in peri-implantitis group (Chao1 index: 236.85±66.13 vs. 150.54±57.43, P < 0.001; Shannon index: 3.42±0.48 vs. 3.02±0.65, P=0.032). Principal coordinated analysis showed that the submucosal microbial structure had significant difference between healthy and peri-implantitis groups [R2=0.243, P=0.001, analysis of similarities (ANOSIM)]. Compared with healthy implants, relative abundance of periodontal pathogens were higher in peri-implantitis, including members of the red complex (Porphyromonas gingivalis, Tannerella forsythia, Treponema denticola) and some members of orange complex (Precotella intermedia, Eubacterium nodatum, Parvimonas micra), as well as some new periodontal pathogens, such as Fillifactor alocis, Fretibacterium fastidiosum, Desulfobulbus sp._HMT_041, and Porphyromonas endodontalis. Spearman correlation analysis revealed that the relative abundance of Treponema denticola (r=0.686, P < 0.001), Tannerella forsythia (r=0.675, P < 0.001), Fretibacterium sp. (r=0.671, P < 0.001), Desulfobulbus sp._HMT_041 (r=0.664, P < 0.001), Filifactor alocis (r=0.642, P < 0.001), Fretibacterium fastidiosum (r=0.604, P < 0.001), Porphyromonas gingivalis (r=0.597, P < 0.001), Porphyromonas endodontalis (r=0.573, P < 0.001) were positive correlated with PPD. While the relative abundance of Rothia aeria (r=-0.615, P < 0.001) showed negatively correlation with PPD. Conclusion: Marked differences were observed in the microbial profiles of healthy implants and peri-implantitis. The members of red and orange complex as well as some new periodontal pathogens seem to play an important role in peri-implant disease. Compared with healthy implants, the submucosal microbial of peri-implantitis were characterized by high species richness and diversity.

Key words: Dental implants, Peri-implantitis, Human microbiota, Illumina sequencing

CLC Number: 

  • R781.4

Table 1

Characteristics of subjects and implants"

Parameters Healthy implants (n=20) Peri-implantitis (n=29) F value χ2 P value
Age/years 47.6±15.0 54.7±12.9 0.478 0.086
Gender (male/female) 8/12 17/12 0.037 0.208
Position
    Anterior maxilla 3 (15.0) 2 (6.9) 1.073 0.784
    Posterior maxilla 7 (35.0) 10 (34.5)
    Anterior mandibula 1 (5.0) 1 (3.4)
    Posterior mandibula 9 (45.0) 16 (55.2)
Mean PLI 0.20±0.34 1.57±0.78 < 0.001
Mean PPD/mm 2.36±0.25 6.20±1.64 30.324 < 0.001
Mean BI 0.14±0.20 2.86±0.72 14.158 < 0.001
Suppuration 0 13 (44.8) 12.203 < 0.001
Mean MBL/mm 0 3.12±1.79 26.634 < 0.001

Figure 1

Rarefaction curves based on Sobs index (observed OTU) OTU, operational taxonomic units."

Figure 2

Microbial component at phyla and genus level of submucosal microbial in peri-implantitis and health implants A, at the phylum level; B, at the genus level."

Figure 3

Comparison the α diversity of submucosal microbial in peri-implantitis and health implants A, microbial richness presented by Chao1 index; B, microbial diversity presented by Shannon index. *P < 0.05, ***P < 0.001, Wilcoxon rank-sum test."

Figure 4

Comparison the β diversity of submucosal microbial in peri-implantitis and health implants ANOSIM, analysis of similarities; PC, principal component."

Figure 5

Comparison the component difference of submucosal microbial in peri-implantitis and health implants A, at the phylum level; B, top 15 most abundant genera; C, top 15 most abundant species. Only taxa that were significantly different between the peri-implantitis and health implants group were plotted (Wilcoxon rank-sum test and FDR-adjusted P < 0.05). FDR, false discovery rate."

Figure 6

Species showed significant correlation with PPD in submucosal microbial of peri-implants Only species with |Spearman correlation coefficient| > 0.5 and P < 0.05 were plotted. PPD, probing pocket depth."

1 Howe MS , Keys W , Richards D . Long-term (10-year) dental implant survival: A systematic review and sensitivity meta-analysis[J]. J Dent, 2019, 84, 9- 21.
doi: 10.1016/j.jdent.2019.03.008
2 Schwarz F , Derks J , Monje A , et al. Peri-implantitis[J]. J Periodontol, 2018, 89 (Suppl 1): S267- S290.
3 Kordbacheh Changi K , Finkelstein J , Papapanou PN . Peri-implan-titis prevalence, incidence rate, and risk factors: A study of electronic health records at a U.S. dental school[J]. Clin Oral Implants Res, 2019, 30 (4): 306- 314.
doi: 10.1111/clr.13416
4 Berglundh T , Armitage G , Araujo MG , et al. 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[J]. J Clin Periodontol, 2018, 45 (Suppl 20): S286- S291.
5 Renvert S , Persson GR , Pirih FQ , et al. Peri-implant health, peri-implant mucositis, and peri-implantitis: Case definitions and diagnostic considerations[J]. J Periodontol, 2018, 89 (Suppl 1): S304- S312.
6 Araujo MG , Lindhe J . Peri-implant health[J]. J Clin Periodontol, 2018, 45 (Suppl 20): S230- S236.
7 孙菲, 李思琪, 危伊萍, 等. 种植体周病非手术治疗中联合应用甘氨酸粉喷砂的临床效果评价[J]. 北京大学学报(医学版), 2022, 54 (1): 119- 125.
doi: 10.19723/j.issn.1671-167X.2022.01.019
8 de Waal YC , Eijsbouts HV , Winkel EG , et al. Microbial characteristics of peri-implantitis: A case-control study[J]. J Periodontol, 2017, 88 (2): 209- 217.
doi: 10.1902/jop.2016.160231
9 Paster BJ , Olsen I , Aas JA , et al. The breadth of bacterial diversity in the human periodontal pocket and other oral sites[J]. Periodontology 2000, 2006, 42 (1): 80- 87.
doi: 10.1111/j.1600-0757.2006.00174.x
10 Renvert S , Roos-Jansaker AM , Lindahl C , et al. Infection at titanium implants with or without a clinical diagnosis of inflammation[J]. Clin Oral Implants Res, 2007, 18 (4): 509- 516.
doi: 10.1111/j.1600-0501.2007.01378.x
11 Zheng H , Xu L , Wang Z , et al. Subgingival microbiome in patients with healthy and ailing dental implants[J]. Sci Rep, 2015, 5, 10948.
doi: 10.1038/srep10948
12 Sanz-Martin I , Doolittle-Hall J , Teles RP , et al. Exploring the microbiome of healthy and diseased peri-implant sites using Illumina sequencing[J]. J Clin Periodontol, 2017, 44 (12): 1274- 1284.
doi: 10.1111/jcpe.12788
13 Nie J , Zhang Q , Zheng H , et al. Pyrosequencing of the subgingival microbiome in peri-implantitis after non-surgical mechanical debridement therapy[J]. J Periodontal Res, 2020, 55 (2): 238- 246.
doi: 10.1111/jre.12708
14 Socransky SS , Haffajee AD , Cugini MA , et al. Microbial complexes in subgingival plaque[J]. J Clin Periodontol, 1998, 25 (2): 134- 144.
doi: 10.1111/j.1600-051X.1998.tb02419.x
15 Al-Ahmad A , Muzafferiy F , Anderson AC , et al. Shift of micro-bial composition of peri-implantitis-associated oral biofilm as revealed by 16S rRNA gene cloning[J]. J Med Microbiol, 2018, 67 (3): 332- 340.
doi: 10.1099/jmm.0.000682
16 da Silva ES , Feres M , Figueiredo LC , et al. Microbiological diversity of peri-implantitis biofilm by Sanger sequencing[J]. Clin Oral Implants Res, 2014, 25 (10): 1192- 1199.
doi: 10.1111/clr.12231
17 Oliveira RR , Fermiano D , Feres M , et al. Levels of candidate periodontal pathogens in subgingival biofilm[J]. J Dent Res, 2016, 95 (6): 711- 718.
doi: 10.1177/0022034516634619
18 Fu JH , Wang HL . Breaking the wave of peri-implantitis[J]. Periodontol 2000, 2020, 84 (1): 145- 160.
doi: 10.1111/prd.12335
19 Perez-Chaparro PJ , Duarte PM , Shibli JA , et al. The current weight of evidence of the microbiologic profile associated with peri-implantitis: A systematic review[J]. J Periodontol, 2016, 87 (11): 1295- 1304.
doi: 10.1902/jop.2016.160184
20 Kroger A , Hulsmann C , Fickl S , et al. The severity of human peri-implantitis lesions correlates with the level of submucosal microbial dysbiosis[J]. J Clin Periodontol, 2018, 45 (12): 1498- 1509.
doi: 10.1111/jcpe.13023
21 Galofré M , Palao D , Vicario M , et al. Clinical and microbiological evaluation of the effect of Lactobacillus reuteri in the treatment of mucositis and peri-implantitis: A triple-blind randomized clinical trial[J]. J Periodontal Res, 2018, 53 (3): 378- 390.
doi: 10.1111/jre.12523
22 Mombelli A . Maintenance therapy for teeth and implants[J]. Periodontol 2000, 2019, 79 (1): 190- 199.
doi: 10.1111/prd.12255
23 Berglundh T , Jepsen S , Stadlinger B , et al. Peri-implantitis and its prevention[J]. Clin Oral Implants Res, 2019, 30 (2): 150- 155.
doi: 10.1111/clr.13401
24 Mombelli A . Microbial colonization of the periodontal pocket and its significance for periodontal therapy[J]. Periodontol 2000, 2018, 76 (1): 85- 96.
doi: 10.1111/prd.12147
[1] Congwei WANG,Min GAO,Yao YU,Wenbo ZHANG,Xin PENG. Clinical analysis of denture rehabilitation after mandibular fibula free-flap reconstruction [J]. Journal of Peking University (Health Sciences), 2024, 56(1): 66-73.
[2] Qian DING,Wen-jin LI,Feng-bo SUN,Jing-hua GU,Yuan-hua LIN,Lei ZHANG. Effects of surface treatment on the phase and fracture strength of yttria- and magnesia-stabilized zirconia implants [J]. Journal of Peking University (Health Sciences), 2023, 55(4): 721-728.
[3] Ling-wei MENG,Xue LI,Sheng-han GAO,Yue LI,Rui-tao CAO,Yi ZHANG,Shao-xia PAN. Comparison of three methods for establishing rat peri-implantitis model [J]. Journal of Peking University (Health Sciences), 2023, 55(1): 22-29.
[4] LI Yi,YU Hua-jie,QIU Li-xin. Clinical classification and treatment decision of implant fracture [J]. Journal of Peking University (Health Sciences), 2022, 54(1): 126-133.
[5] Fei SUN,Si-qi LI,Yi-ping WEI,Jin-sheng ZHONG,Cui WANG,Wen-jie HU. Efficacy of combined application of glycine powder air-polishing in non-surgical treatment of peri-implant diseases [J]. Journal of Peking University (Health Sciences), 2022, 54(1): 119-125.
[6] LI Peng,PIAO Mu-zi,HU Hong-cheng,WANG Yong,ZHAO Yi-jiao,SHEN Xiao-jing. Radiography study on osteotome sinus floor elevation with placed implant simultaneously with no graft augmentation [J]. Journal of Peking University (Health Sciences), 2021, 53(1): 95-101.
[7] Zhong ZHANG,Huan-xin MENG,Jie HAN,Li ZHANG,Dong SHI. Effect of vertical soft tissue thickness on clinical manifestation of peri-implant tissue in patients with periodontitis [J]. Journal of Peking University (Health Sciences), 2020, 52(2): 332-338.
[8] Dong SHI,Jie CAO,Shi-ai DAI,Huan-xin MENG. Short-term outcome of regenerative surgery treating peri-implantitis [J]. Journal of Peking University(Health Sciences), 2020, 52(1): 58-63.
[9] Chun-ping LIN,Song-he LU,Jun-xin ZHU,Hong-cheng HU,Zhao-guo YUE,Zhi-hui TANG. Influence of thread shapes of custom-made root-analogue implants on stress distribution of peri-implant bone: A three-dimensional finite element analysis [J]. Journal of Peking University(Health Sciences), 2019, 51(6): 1130-1137.
[10] Qian WANG,Dan LI,Zhi-hui TANG. Sinus floor elevation and simultaneous dental implantation: A long term retrospective study of sinus bone gain [J]. Journal of Peking University(Health Sciences), 2019, 51(5): 925-930.
[11] Xiao-qian LIU,Qiu-wen CHEN,Hai-lan FENG,Bing WANG,Jian QU,Zhen SUN,Mo-di HENG,Shao-xia PAN. Oral hygiene maintenance of locator attachments implant overdentures in edentulous population: A longitudinal study [J]. Journal of Peking University(Health Sciences), 2019, 51(1): 136-144.
[12] Zhi-yong△ ZHANG,Tian MENG,Quan CHEN,Wen-shu LIU,Yu-huan CHEN. Retrospective analysis of early dental implant failure [J]. Journal of Peking University(Health Sciences), 2018, 50(6): 1088-1091.
[13] ZHANG Hai-dong, ZHANG Li, SHI Dong, HAN Jie, YAN Xia, XIE Ye-si, MENG Huan-xin. Clinical study of locking-taper implants in patients treated for periodontitis [J]. Journal of Peking University(Health Sciences), 2018, 50(2): 300-307.
[14] LIU Jing-yin, CHEN Fei, GE Yan-jun, WEI Ling, PAN Shao-xia, FENG Hai-lan. Influence of implants prepared by selective laser melting on early bone healing [J]. Journal of Peking University(Health Sciences), 2018, 50(1): 117-122.
[15] LIANG Nai-wen, SHI Lei，HUANG Ying，DENG Xu-liang. Role of different scale structures of titanium implant in the biological behaviors of human umbilical vein endothelial cells [J]. Journal of Peking University(Health Sciences), 2017, 49(1): 43-048.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
Copyright © Journal of Peking University (Health Sciences), All Rights Reserved.
Powered by Beijing Magtech Co. Ltd