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Metagenomic analysis examines oral microbiome changes and interplay with immune response following prenatal total oral rehabilitation

BACKGROUND: Suboptimal maternal oral health during pregnancy is potentially associated with adverse birth outcomes and increased dental caries risks in children. This study aimed to assess the oral microbiome and immune response following an innovative clinical regimen, Prenatal Total Oral Rehabilit...

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Autores principales: Wu, Tong Tong, Sohn, Michael, Manning, Samantha, Beblavy, Robert, Gill, Steven, Quataert, Sally, Vasani, Shruti, Jang, Hoonji, Zeng, Yan, Bruno, Jennifer, Vazquez, Adriana, Fiscella, Kevin, Xiao, Jin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9985285/
https://www.ncbi.nlm.nih.gov/pubmed/36871005
http://dx.doi.org/10.1186/s12967-023-03997-9
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author Wu, Tong Tong
Sohn, Michael
Manning, Samantha
Beblavy, Robert
Gill, Steven
Quataert, Sally
Vasani, Shruti
Jang, Hoonji
Zeng, Yan
Bruno, Jennifer
Vazquez, Adriana
Fiscella, Kevin
Xiao, Jin
author_facet Wu, Tong Tong
Sohn, Michael
Manning, Samantha
Beblavy, Robert
Gill, Steven
Quataert, Sally
Vasani, Shruti
Jang, Hoonji
Zeng, Yan
Bruno, Jennifer
Vazquez, Adriana
Fiscella, Kevin
Xiao, Jin
author_sort Wu, Tong Tong
collection PubMed
description BACKGROUND: Suboptimal maternal oral health during pregnancy is potentially associated with adverse birth outcomes and increased dental caries risks in children. This study aimed to assess the oral microbiome and immune response following an innovative clinical regimen, Prenatal Total Oral Rehabilitation (PTOR), that fully restores women’s oral health to a “disease-free status” before delivery. METHODS: This prospective cohort study assessed 15 pregnant women at baseline and 3 follow-up visits (1 week, 2 weeks, and 2 months) after receiving PTOR. The salivary and supragingival plaque microbiomes were analyzed using metagenomic sequencing. Multiplexed Luminex cytokine assays were performed to examine immune response following PTOR. The association between salivary immune markers and oral microbiome was further examined. RESULTS: PTOR was associated with a reduction of periodontal pathogens in plaque, for instance, a lower relative abundance of Tannerella forsythia and Treponema denticola at 2 weeks compared to the baseline (p < 0.05). The alpha diversity of plaque microbial community was significantly reduced at the 1-week follow-up (p < 0.05). Furthermore, we observed significant changes in the Actinomyces defective-associated carbohydrate degradation pathway and Streptococcus Gordonii-associated fatty acid biosynthesis pathway. Two immune markers related to adverse birth outcomes significantly differed between baseline and follow-up. ITAC, negatively correlated with preeclampsia severity, significantly increased at 1-week follow-up; MCP-1, positively correlated with gestational age, was elevated at 1-week follow-up. Association modeling between immune markers and microbiome further revealed specific oral microorganisms that are potentially correlated with the host immune response. CONCLUSIONS: PTOR is associated with alteration of the oral microbiome and immune response among a cohort of underserved US pregnant women. Future randomized clinical trials are warranted to comprehensively assess the impact of PTOR on maternal oral flora, birth outcomes, and their offspring’s oral health. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12967-023-03997-9.
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spelling pubmed-99852852023-03-05 Metagenomic analysis examines oral microbiome changes and interplay with immune response following prenatal total oral rehabilitation Wu, Tong Tong Sohn, Michael Manning, Samantha Beblavy, Robert Gill, Steven Quataert, Sally Vasani, Shruti Jang, Hoonji Zeng, Yan Bruno, Jennifer Vazquez, Adriana Fiscella, Kevin Xiao, Jin J Transl Med Research BACKGROUND: Suboptimal maternal oral health during pregnancy is potentially associated with adverse birth outcomes and increased dental caries risks in children. This study aimed to assess the oral microbiome and immune response following an innovative clinical regimen, Prenatal Total Oral Rehabilitation (PTOR), that fully restores women’s oral health to a “disease-free status” before delivery. METHODS: This prospective cohort study assessed 15 pregnant women at baseline and 3 follow-up visits (1 week, 2 weeks, and 2 months) after receiving PTOR. The salivary and supragingival plaque microbiomes were analyzed using metagenomic sequencing. Multiplexed Luminex cytokine assays were performed to examine immune response following PTOR. The association between salivary immune markers and oral microbiome was further examined. RESULTS: PTOR was associated with a reduction of periodontal pathogens in plaque, for instance, a lower relative abundance of Tannerella forsythia and Treponema denticola at 2 weeks compared to the baseline (p < 0.05). The alpha diversity of plaque microbial community was significantly reduced at the 1-week follow-up (p < 0.05). Furthermore, we observed significant changes in the Actinomyces defective-associated carbohydrate degradation pathway and Streptococcus Gordonii-associated fatty acid biosynthesis pathway. Two immune markers related to adverse birth outcomes significantly differed between baseline and follow-up. ITAC, negatively correlated with preeclampsia severity, significantly increased at 1-week follow-up; MCP-1, positively correlated with gestational age, was elevated at 1-week follow-up. Association modeling between immune markers and microbiome further revealed specific oral microorganisms that are potentially correlated with the host immune response. CONCLUSIONS: PTOR is associated with alteration of the oral microbiome and immune response among a cohort of underserved US pregnant women. Future randomized clinical trials are warranted to comprehensively assess the impact of PTOR on maternal oral flora, birth outcomes, and their offspring’s oral health. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12967-023-03997-9. BioMed Central 2023-03-04 /pmc/articles/PMC9985285/ /pubmed/36871005 http://dx.doi.org/10.1186/s12967-023-03997-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Wu, Tong Tong
Sohn, Michael
Manning, Samantha
Beblavy, Robert
Gill, Steven
Quataert, Sally
Vasani, Shruti
Jang, Hoonji
Zeng, Yan
Bruno, Jennifer
Vazquez, Adriana
Fiscella, Kevin
Xiao, Jin
Metagenomic analysis examines oral microbiome changes and interplay with immune response following prenatal total oral rehabilitation
title Metagenomic analysis examines oral microbiome changes and interplay with immune response following prenatal total oral rehabilitation
title_full Metagenomic analysis examines oral microbiome changes and interplay with immune response following prenatal total oral rehabilitation
title_fullStr Metagenomic analysis examines oral microbiome changes and interplay with immune response following prenatal total oral rehabilitation
title_full_unstemmed Metagenomic analysis examines oral microbiome changes and interplay with immune response following prenatal total oral rehabilitation
title_short Metagenomic analysis examines oral microbiome changes and interplay with immune response following prenatal total oral rehabilitation
title_sort metagenomic analysis examines oral microbiome changes and interplay with immune response following prenatal total oral rehabilitation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9985285/
https://www.ncbi.nlm.nih.gov/pubmed/36871005
http://dx.doi.org/10.1186/s12967-023-03997-9
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