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量化舌部和唾液微生物群中与牙周炎相关的口腔微生物失调——综合数据分析

Quantifying periodontitis-associated oral dysbiosis in tongue and saliva microbiomes-An integrated data analysis.

作者信息

Chew Ren Jie Jacob, Tan Kai Soo, Chen Tsute, Al-Hebshi Nezar Noor, Goh Charlene Enhui

机构信息

Faculty of Dentistry, National University of Singapore, Singapore, Singapore.

The Forsyth Institute, Cambridge, Massachusetts, USA.

出版信息

J Periodontol. 2025 Jan;96(1):55-66. doi: 10.1002/JPER.24-0120. Epub 2024 Jul 15.

Abstract

BACKGROUND

Periodontitis is primarily driven by subgingival biofilm dysbiosis. However, the quantification and impact of this periodontal dysbiosis on other oral microbial niches remain unclear. This study seeks to quantify the dysbiotic changes in tongue and salivary microbiomes resulting from periodontitis by applying a clinically relevant dysbiosis index to an integrated data analysis.

METHODS

The National Center for Biotechnology Information (NCBI) database was searched to identify BioProjects with published studies on salivary and tongue microbiomes of healthy and periodontitis subjects. Raw sequence datasets were processed using a standardized bioinformatic pipeline and categorized by their ecological niche and periodontal status. The subgingival microbial dysbiosis index (SMDI), a dysbiosis index originally developed using the subgingival microbiome, was computed at species and genus levels and customized for each niche. Its diagnostic accuracy for periodontitis was evaluated using receiver operating characteristic curves.

RESULTS

Four studies, contributing 328 microbiome samples, were included. At both species and genus levels, periodontitis samples had a higher SMDI, but the differences were only significant for subgingival biofilm and saliva (p < 0.001). However, SMDI showed good diagnostic accuracy for periodontitis status for all three niches (area under curve ranging from 0.76 to 0.90, p < 0.05). The dysbiosis index of subgingival biofilm was positively correlated with saliva consistently (p < 0.001) and with the tongue at the genus level (p = 0.036).

CONCLUSIONS

While the impact on the tongue microbiome requires further investigation, periodontitis-associated dysbiosis affects the salivary microbiome and is quantifiable using the dysbiosis index. The diagnostic potential of salivary microbial dysbiosis as a convenient periodontal biomarker for assessing periodontal status has potential public health and clinical applications.

PLAIN LANGUAGE SUMMARY

Periodontitis, a severe inflammation of the gums which causes bone loss, is a disease caused by an imbalance of good and bad bacteria under the gums. However, it is unclear how this bacterial imbalance in the gums affects the bacterial balance of other distinct parts of the mouth, such as the saliva and tongue. This study uses bacteria datasets of four previously published studies, contributing a total of 328 bacterial samples. The data were processed using a uniform data analysis workflow, and a bacterial score, the subgingival microbial dysbiosis index (SMDI), previously shown to capture periodontitis-associated bacteria imbalance, was calculated separately for samples from under the gums, the saliva, and the tongue. The SMDI was able to distinguish between health and periodontitis within each oral location, and in general, the scores were higher for periodontitis samples, though this difference was significant only for bacteria under the gums and in saliva. Saliva scores were also consistently correlated with bacteria under the gums. This study shows that periodontitis-associated bacterial imbalances are observed in oral locations beyond just under the gums, particularly the saliva. Thus, saliva bacteria may be used as a convenient biomarker for assessing gum disease, allowing for potential public health and clinical applications.

摘要

背景

牙周炎主要由龈下生物膜生态失调引起。然而,这种牙周生态失调对其他口腔微生物生态位的量化及影响仍不清楚。本研究旨在通过将临床相关的生态失调指数应用于综合数据分析,量化牙周炎导致的舌部和唾液微生物群的失调变化。

方法

检索美国国立生物技术信息中心(NCBI)数据库,以识别有关健康和牙周炎受试者唾液及舌部微生物群的已发表研究的生物项目。原始序列数据集使用标准化生物信息学流程进行处理,并按其生态位和牙周状况分类。龈下微生物失调指数(SMDI)是最初使用龈下微生物群开发的一种失调指数,在物种和属水平上进行计算,并针对每个生态位进行定制。使用受试者工作特征曲线评估其对牙周炎的诊断准确性。

结果

纳入了四项研究,共328个微生物群样本。在物种和属水平上,牙周炎样本的SMDI均较高,但差异仅在龈下生物膜和唾液中显著(p<0.001)。然而,SMDI对所有三个生态位的牙周炎状态均显示出良好的诊断准确性(曲线下面积范围为0.76至0.90,p<0.05)。龈下生物膜的失调指数与唾液始终呈正相关(p<0.001),在属水平上与舌部呈正相关(p=0.036)。

结论

虽然对舌部微生物群的影响需要进一步研究,但牙周炎相关的失调会影响唾液微生物群,并且可以使用失调指数进行量化。唾液微生物失调作为一种方便的牙周生物标志物用于评估牙周状况的诊断潜力具有潜在的公共卫生和临床应用价值。

通俗易懂的总结

牙周炎是一种导致骨质流失的严重牙龈炎症,是由牙龈下有益菌和有害菌失衡引起的疾病。然而,尚不清楚牙龈中的这种细菌失衡如何影响口腔其他不同部位(如唾液和舌头)的细菌平衡。本研究使用了四项先前发表研究的细菌数据集,共328个细菌样本。数据使用统一的数据分析工作流程进行处理,并分别为牙龈下、唾液和舌部的样本计算了一个细菌评分,即龈下微生物失调指数(SMDI),该指数先前已被证明可捕捉与牙周炎相关的细菌失衡。SMDI能够区分每个口腔部位的健康和牙周炎情况,一般来说,牙周炎样本的评分更高,不过这种差异仅在牙龈下和唾液中的细菌中显著。唾液评分也始终与牙龈下的细菌相关。这项研究表明,牙周炎相关的细菌失衡不仅在牙龈下,特别是在唾液中也有观察到。因此,唾液细菌可作为评估牙龈疾病的方便生物标志物,具有潜在的公共卫生和临床应用价值。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/479c/11787769/c3cd6d67a020/JPER-96-55-g003.jpg

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