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绝经前和绝经后女性的龈下微生物谱:与血清雌二醇水平的关联。

Subgingival microbial profiles in pre- and postmenopausal women: Associations with serum estradiol levels.

作者信息

Yakar Nil, Yilmaz Busra, Emingil Gulnur, Chen Tsute, Ozdemir Guven, Kantarci Alpdogan

机构信息

The ADA Forsyth Institute, Cambridge, Massachusetts, USA.

Faculty of Science, Department of Biology, Basic and Industrial Microbiology Section, Ege University, Izmir, Turkey.

出版信息

J Periodontol. 2025 Jan;96(1):97-108. doi: 10.1002/JPER.24-0267. Epub 2024 Jul 14.

DOI:10.1002/JPER.24-0267
PMID:39003582
Abstract

BACKGROUND

Subgingival dental plaque is an ecosystem playing a key role in supporting both oral health and systemic health. Menopause-related changes have the potential to disrupt its balance, which is crucial to postmenopausal well-being. Our study explored how circulating estradiol levels correlate with subgingival microbial composition using checkerboard DNA-DNA hybridization in premenopausal and postmenopausal women. We also demonstrated that combining this method with 16S ribosomal RNA (rRNA) sequencing insights remains valuable for examining subgingival ecology.

METHODS

We assessed 40 bacterial species in 77 premenopausal and 81 postmenopausal women using checkerboard DNA-DNA hybridization and measured serum estradiol with enzyme-linked immunosorbent assay (ELISA). Women were categorized by subgingival dysbiosis severity using a modified Subgingival Microbial Dysbiosis Index (mSMDI). Six women from each normobiotic and dysbiotic subgroup across premenopausal and postmenopausal women underwent 16S rRNA sequencing analysis.

RESULTS

DNA checkerboard analysis revealed that most observed variability in individual bacterial proportions is associated with periodontitis. Two species, Leptotrichia buccalis and Streptococcus constellatus, exhibited differences related to estradiol levels within the premenopausal group (p = 0.055 and p = 0.009, respectively). 16S rRNA sequencing confirmed the mSMDI's validity in categorizing normobiotic and dysbiotic states. Menopausal status was not associated with a dysbiotic shift in the subgingival microbiome despite significantly more attachment loss in postmenopausal compared to premenopausal women.

CONCLUSIONS

Our results indicate that decreased estradiol levels or increased attachment loss during menopause are not associated with changes in species abundance or dysbiotic shifts in women. The mSMDI may be a useful tool for classifying subgingival ecology based on its normobiotic or dysbiotic inclination.

PLAIN LANGUAGE SUMMARY

The microorganisms in the oral cavity, particularly those around the teeth and gums, form a complex community known as subgingival plaque. This ecosystem is crucial for maintaining both gum health and systemic health. While disease-related (dysbiotic) subgingival plaque causes gum disease (periodontitis), periodontitis further sustains a dysbiotic subgingival plaque microbial environment. Factors such as hormone levels can potentially influence the balance between health and disease-related subgingival plaque microorganisms. We investigated whether blood estradiol levels in women affect the abundance of specific bacteria in subgingival plaque and whether menopause alters the microbial balance in this community. We found that two bacterial species, Leptotrichia buccalis and Streptococcus constellatus, were positively associated with estradiol levels, but only in premenopausal women. Despite postmenopausal women having more severe periodontitis, their subgingival microbiome did not exhibit more dysbiotic characteristics than that of premenopausal women.

摘要

背景

龈下牙菌斑是一个生态系统,在维持口腔健康和全身健康方面发挥着关键作用。绝经相关变化可能会破坏其平衡,而这种平衡对绝经后健康至关重要。我们的研究利用棋盘式DNA-DNA杂交技术,探讨了绝经前和绝经后女性循环雌二醇水平与龈下微生物组成之间的相关性。我们还证明,将该方法与16S核糖体RNA(rRNA)测序相结合,对于研究龈下生态仍然具有重要价值。

方法

我们使用棋盘式DNA-DNA杂交技术评估了77名绝经前和81名绝经后女性的40种细菌,并通过酶联免疫吸附测定(ELISA)法测量血清雌二醇水平。使用改良的龈下微生物失调指数(mSMDI)对女性的龈下失调严重程度进行分类。从绝经前和绝经后女性的每个正常生物群和失调生物群亚组中选取6名女性进行16S rRNA测序分析。

结果

DNA棋盘分析显示,个体细菌比例中观察到的大多数变异性与牙周炎有关。两种细菌,即颊纤毛菌和星座链球菌,在绝经前组中表现出与雌二醇水平相关的差异(分别为p = 0.055和p = 0.009)。16S rRNA测序证实了mSMDI在对正常生物群和失调生物群状态进行分类方面的有效性。尽管绝经后女性的附着丧失明显多于绝经前女性,但绝经状态与龈下微生物群的失调转变无关。

结论

我们的结果表明,绝经期间雌二醇水平降低或附着丧失增加与女性物种丰度变化或失调转变无关。mSMDI可能是一种基于其正常生物群或失调生物群倾向来分类龈下生态的有用工具。

通俗易懂的总结

口腔中的微生物,特别是牙齿和牙龈周围的微生物,形成了一个复杂的群落,称为龈下菌斑。这个生态系统对于维持牙龈健康和全身健康至关重要。虽然与疾病相关(失调)的龈下菌斑会导致牙龈疾病(牙周炎),但牙周炎会进一步维持失调的龈下菌斑微生物环境。激素水平等因素可能会影响与健康和疾病相关的龈下菌斑微生物之间的平衡。我们研究了女性血液中的雌二醇水平是否会影响龈下菌斑中特定细菌的丰度,以及绝经是否会改变这个群落中的微生物平衡。我们发现,两种细菌,即颊纤毛菌和星座链球菌,与雌二醇水平呈正相关,但仅在绝经前女性中如此。尽管绝经后女性的牙周炎更严重,但其龈下微生物群并未表现出比绝经前女性更多的失调特征。

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