Relationship Between the Salivary Microbiome and Oral Malodor Metabolites in Older Thai Individuals with Periodontitis and the Cytotoxic Effects of Malodor Compounds on Human Oral Squamous Carcinoma (HSC-4) Cells

<b>Background/Objectives</b>: Halitosis is primarily caused by the activity of oral microorganisms. In this study, we employed metagenomic sequencing and metabolomic approaches to investigate the differences in salivary microbiota and metabolite profiles between individuals with halitosi...

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Main Authors: Witsanu Srila, Kritsana Sripilai, Thunwa Binlateh, Peungchaleoy Thammanichanon, Watcharaphol Tiskratok, Parinya Noisa, Paiboon Jitprasertwong
Format: Article
Language:English
Published: MDPI AG 2025-01-01
Series:Dentistry Journal
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Online Access:https://www.mdpi.com/2304-6767/13/1/36
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author Witsanu Srila
Kritsana Sripilai
Thunwa Binlateh
Peungchaleoy Thammanichanon
Watcharaphol Tiskratok
Parinya Noisa
Paiboon Jitprasertwong
author_facet Witsanu Srila
Kritsana Sripilai
Thunwa Binlateh
Peungchaleoy Thammanichanon
Watcharaphol Tiskratok
Parinya Noisa
Paiboon Jitprasertwong
author_sort Witsanu Srila
collection DOAJ
description <b>Background/Objectives</b>: Halitosis is primarily caused by the activity of oral microorganisms. In this study, we employed metagenomic sequencing and metabolomic approaches to investigate the differences in salivary microbiota and metabolite profiles between individuals with halitosis and periodontitis and healthy controls. Additionally, we expanded the study to examine how oral malodorous compounds interact with human oral squamous carcinoma (HSC-4) cells. <b>Methods</b>: Saliva samples were collected and analyzed using Ultra-High Performance Liquid Chromatography–Mass Spectrometry (UHPLC-MS) to identify metabolites. We then assessed the correlations between the microbiota and metabolites. Furthermore, the impact of oral malodorous substances on HSC-4 cells was investigated by evaluating apoptosis, antioxidant activity, and inflammatory properties. <b>Results:</b> The microbiota and metabolite profiles showed significant differences between the halitosis with periodontitis group and the periodontally healthy group. The halitosis with periodontitis group exhibited significantly higher relative abundances of eight genera: <i>Tannerella</i>, <i>Selenomonas</i>, <i>Bacteroides</i>, <i>Filifactor</i>, <i>Phocaeicola</i>, <i>Fretibacterium</i>, <i>Eubacterium saphenum</i>, and <i>Desulfobulbus</i>. In contrast, the periodontally healthy group showed significantly higher relative abundances of Family <i>XIII UCG-001</i>, <i>Haemophilus</i>, and <i>Streptobacillus</i>. Two metabolites, 2,3-dihydro-1H-indole and 10,11-dihydro-12R-hydroxy-leukotriene E4, were significantly higher in individuals with halitosis and periodontitis. In the treatment of HSC-4 cells with metabolites, dimethyl sulfide (DMS) did not show significant effects while indole appeared to induce cell death in HSC-4 cells by triggering apoptotic pathways. Additionally, both indole and DMS affected the inflammatory and antioxidant properties of HSC-4 cells. <b>Conclusions</b>: This study provides insights into the mechanisms of halitosis by exploring the correlations between microbiota and metabolite profiles. Furthermore, oral metabolites were shown to impact the cellular response of HSC-4 cells.
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spelling doaj-art-0985c6ccb3dc4a2cb3c27db9b64273a82025-01-24T13:28:43ZengMDPI AGDentistry Journal2304-67672025-01-011313610.3390/dj13010036Relationship Between the Salivary Microbiome and Oral Malodor Metabolites in Older Thai Individuals with Periodontitis and the Cytotoxic Effects of Malodor Compounds on Human Oral Squamous Carcinoma (HSC-4) CellsWitsanu Srila0Kritsana Sripilai1Thunwa Binlateh2Peungchaleoy Thammanichanon3Watcharaphol Tiskratok4Parinya Noisa5Paiboon Jitprasertwong6Division of Biology, Faculty of Science and Technology, Rajamangala University of Technology Thanyaburi, Pathum Thani 12110, ThailandLaboratory of Cell-Based Assays and Innovations, School of Biotechnology, Institute of Agricultural Technology, Suranaree University of Technology, Nakhon Ratchasima 30000, ThailandSchool of Pharmacy, Walailak University, Nakhon Si Thammarat 80160, ThailandInstitute of Dentistry, Suranaree University of Technology, Nakhon Ratchasima 30000, ThailandInstitute of Dentistry, Suranaree University of Technology, Nakhon Ratchasima 30000, ThailandLaboratory of Cell-Based Assays and Innovations, School of Biotechnology, Institute of Agricultural Technology, Suranaree University of Technology, Nakhon Ratchasima 30000, ThailandInstitute of Dentistry, Suranaree University of Technology, Nakhon Ratchasima 30000, Thailand<b>Background/Objectives</b>: Halitosis is primarily caused by the activity of oral microorganisms. In this study, we employed metagenomic sequencing and metabolomic approaches to investigate the differences in salivary microbiota and metabolite profiles between individuals with halitosis and periodontitis and healthy controls. Additionally, we expanded the study to examine how oral malodorous compounds interact with human oral squamous carcinoma (HSC-4) cells. <b>Methods</b>: Saliva samples were collected and analyzed using Ultra-High Performance Liquid Chromatography–Mass Spectrometry (UHPLC-MS) to identify metabolites. We then assessed the correlations between the microbiota and metabolites. Furthermore, the impact of oral malodorous substances on HSC-4 cells was investigated by evaluating apoptosis, antioxidant activity, and inflammatory properties. <b>Results:</b> The microbiota and metabolite profiles showed significant differences between the halitosis with periodontitis group and the periodontally healthy group. The halitosis with periodontitis group exhibited significantly higher relative abundances of eight genera: <i>Tannerella</i>, <i>Selenomonas</i>, <i>Bacteroides</i>, <i>Filifactor</i>, <i>Phocaeicola</i>, <i>Fretibacterium</i>, <i>Eubacterium saphenum</i>, and <i>Desulfobulbus</i>. In contrast, the periodontally healthy group showed significantly higher relative abundances of Family <i>XIII UCG-001</i>, <i>Haemophilus</i>, and <i>Streptobacillus</i>. Two metabolites, 2,3-dihydro-1H-indole and 10,11-dihydro-12R-hydroxy-leukotriene E4, were significantly higher in individuals with halitosis and periodontitis. In the treatment of HSC-4 cells with metabolites, dimethyl sulfide (DMS) did not show significant effects while indole appeared to induce cell death in HSC-4 cells by triggering apoptotic pathways. Additionally, both indole and DMS affected the inflammatory and antioxidant properties of HSC-4 cells. <b>Conclusions</b>: This study provides insights into the mechanisms of halitosis by exploring the correlations between microbiota and metabolite profiles. Furthermore, oral metabolites were shown to impact the cellular response of HSC-4 cells.https://www.mdpi.com/2304-6767/13/1/36halitosisperiodontitissalivary microbiomeoral malodorous compoundsalivary metabolomicshuman oral squamous carcinoma cells
spellingShingle Witsanu Srila
Kritsana Sripilai
Thunwa Binlateh
Peungchaleoy Thammanichanon
Watcharaphol Tiskratok
Parinya Noisa
Paiboon Jitprasertwong
Relationship Between the Salivary Microbiome and Oral Malodor Metabolites in Older Thai Individuals with Periodontitis and the Cytotoxic Effects of Malodor Compounds on Human Oral Squamous Carcinoma (HSC-4) Cells
Dentistry Journal
halitosis
periodontitis
salivary microbiome
oral malodorous compound
salivary metabolomics
human oral squamous carcinoma cells
title Relationship Between the Salivary Microbiome and Oral Malodor Metabolites in Older Thai Individuals with Periodontitis and the Cytotoxic Effects of Malodor Compounds on Human Oral Squamous Carcinoma (HSC-4) Cells
title_full Relationship Between the Salivary Microbiome and Oral Malodor Metabolites in Older Thai Individuals with Periodontitis and the Cytotoxic Effects of Malodor Compounds on Human Oral Squamous Carcinoma (HSC-4) Cells
title_fullStr Relationship Between the Salivary Microbiome and Oral Malodor Metabolites in Older Thai Individuals with Periodontitis and the Cytotoxic Effects of Malodor Compounds on Human Oral Squamous Carcinoma (HSC-4) Cells
title_full_unstemmed Relationship Between the Salivary Microbiome and Oral Malodor Metabolites in Older Thai Individuals with Periodontitis and the Cytotoxic Effects of Malodor Compounds on Human Oral Squamous Carcinoma (HSC-4) Cells
title_short Relationship Between the Salivary Microbiome and Oral Malodor Metabolites in Older Thai Individuals with Periodontitis and the Cytotoxic Effects of Malodor Compounds on Human Oral Squamous Carcinoma (HSC-4) Cells
title_sort relationship between the salivary microbiome and oral malodor metabolites in older thai individuals with periodontitis and the cytotoxic effects of malodor compounds on human oral squamous carcinoma hsc 4 cells
topic halitosis
periodontitis
salivary microbiome
oral malodorous compound
salivary metabolomics
human oral squamous carcinoma cells
url https://www.mdpi.com/2304-6767/13/1/36
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