BackgroundPeriodontitis 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.MethodsThe 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.ResultsFour 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).ConclusionsWhile 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 SUMMARYPeriodontitis, 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.

中文翻译：

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量化舌头和唾液微生物组中与牙周炎相关的口腔生态失调——综合数据分析


背景牙周炎主要是由龈下生物膜失调引起的。然而，这种牙周生态失调对其他口腔微生物生态位的量化和影响仍不清楚。本研究旨在通过将临床相关的菌群失调指数应用于综合数据分析来量化牙周炎引起的舌头和唾液微生物组的菌群失调变化。健康受试者和牙周炎受试者的舌头微生物组。使用标准化生物信息学流程处理原始序列数据集，并根据其生态位和牙周状态进行分类。龈下微生物失调指数（SMDI）是一种最初使用龈下微生物组开发的失调指数，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，提供了 328 个微生物组样本。在种和属水平上，牙周炎样本均具有较高的 SMDI，但差异仅对于龈下生物膜和唾液而言显着（ p < 0.001)。然而，SMDI 对所有三个牙周炎状态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）。龈下生物膜的生态失调指数与唾液始终呈正相关（ p < 0.001）并且舌头处于属水平（ p = 0.036）。结论虽然对舌头微生物群的影响需要进一步研究，但牙周炎相关的菌群失调会影响唾液微生物群，并且可以使用菌群失调指数进行量化。唾液微生物失调作为评估牙周状态的便捷牙周生物标志物的诊断潜力具有潜在的公共卫生和临床应用价值。 通俗语言摘要牙周炎是一种严重的牙龈炎症，会导致骨质流失，是一种由好与坏不平衡引起的疾病牙龈下的细菌。然而，目前尚不清楚牙龈中的细菌失衡如何影响口腔其他不同部位（例如唾液和舌头）的细菌平衡。这项研究使用了之前发表的四项研究的细菌数据集，总共提供了 328 个细菌样本。使用统一的数据分析工作流程处理数据，并分别计算牙龈下、唾液和牙龈下的样本的细菌评分、龈下微生物失调指数（SMDI），之前显示该指数可以捕捉牙周炎相关的细菌失衡。舌头。 SMDI 能够区分每个口腔位置的健康和牙周炎，一般来说，牙周炎样本的得分较高，尽管这种差异仅对牙龈下和唾液中的细菌显着。唾液评分也与牙龈下的细菌一致相关。这项研究表明，在牙龈下方以外的口腔部位，尤其是唾液中，观察到与牙周炎相关的细菌失衡。因此，唾液细菌可以用作评估牙龈疾病的便捷生物标志物，从而具有潜在的公共卫生和临床应用。