Shotgun metagenomic analysis of the oral microbiome in gingivitis: a nested case-control study

Background Gingivitis, i.e. inflammation of the gums, is often induced by dental plaque. However, its exact link to the oral microbiota remains unclear.Methods In a case-control study involving 120 participants, comprising 60 cases and 60 controls (mean age (SD) 36.6 (7.6) years; 50% males), nested...

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Main Authors: Muhammed Manzoor, Jaakko Leskelä, Milla Pietiäinen, Nicolas Martinez-Majander, Eija Könönen, Teemu Niiranen, Leo Lahti, Juha Sinisalo, Jukka Putaala, Pirkko J. Pussinen, Susanna Paju
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Journal of Oral Microbiology
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Online Access:https://www.tandfonline.com/doi/10.1080/20002297.2024.2330867
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author Muhammed Manzoor
Jaakko Leskelä
Milla Pietiäinen
Nicolas Martinez-Majander
Eija Könönen
Teemu Niiranen
Leo Lahti
Juha Sinisalo
Jukka Putaala
Pirkko J. Pussinen
Susanna Paju
author_facet Muhammed Manzoor
Jaakko Leskelä
Milla Pietiäinen
Nicolas Martinez-Majander
Eija Könönen
Teemu Niiranen
Leo Lahti
Juha Sinisalo
Jukka Putaala
Pirkko J. Pussinen
Susanna Paju
author_sort Muhammed Manzoor
collection DOAJ
description Background Gingivitis, i.e. inflammation of the gums, is often induced by dental plaque. However, its exact link to the oral microbiota remains unclear.Methods In a case-control study involving 120 participants, comprising 60 cases and 60 controls (mean age (SD) 36.6 (7.6) years; 50% males), nested within a prospective multicentre cohort study, we examined the oral microbiome composition of gingivitis patients and their controls using shotgun metagenomic sequencing of saliva samples. Participants underwent clinical and radiographic oral health examinations, including bleeding on probing (BOP), at six tooth sites. BOP ≥33% was considered ‘generalized gingivitis/initial periodontitis’(GG/IP), and BOP <33% as ‘healthy and localized gingivitis’(H/LG). Functional potential was inferred using HUMANn3.Results GG/IP exhibited an increase in the abundance of Actinomyces, Porphyromonas, Aggregatibacter, Corynebacterium, Olsenella, and Treponema, whereas H/LG exhibited an increased abundance of Candidatus Nanosynbacter. Nineteen bacterial species and four microbial functional profiles, including L-methionine, glycogen, and inosine-5’-phosphate biosynthesis, were associated with GG/IP. Constructing models with multiple markers resulted in a strong predictive value for GG/IP, with an area under the curve (ROC) of 0.907 (95% CI: 0.848-0.966).Conclusion We observed distinct differences in the oral microbiome between the GG/IP and H/LG groups, indicating similar yet unique microbial profiles and emphasizing their potential role in progression of periodontal diseases.
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spelling doaj-art-d6ab7a99a1b840d1a5d5ad0508ae5d6c2024-11-26T06:52:11ZengTaylor & Francis GroupJournal of Oral Microbiology2000-22972024-12-0116110.1080/20002297.2024.2330867Shotgun metagenomic analysis of the oral microbiome in gingivitis: a nested case-control studyMuhammed Manzoor0Jaakko Leskelä1Milla Pietiäinen2Nicolas Martinez-Majander3Eija Könönen4Teemu Niiranen5Leo Lahti6Juha Sinisalo7Jukka Putaala8Pirkko J. Pussinen9Susanna Paju10Department of Oral and Maxillofacial Diseases, University of Helsinki, Helsinki, FinlandDepartment of Oral and Maxillofacial Diseases, University of Helsinki, Helsinki, FinlandDepartment of Oral and Maxillofacial Diseases, University of Helsinki, Helsinki, FinlandDepartment of Neurology, Helsinki University Hospital and University of Helsinki, Helsinki, FinlandInstitute of Dentistry, University of Turku, Turku, FinlandDepartment of Public Health and Welfare, Finnish Institute for Health and Welfare, Helsinki, FinlandDepartment of Computing, University of Turku, Turku, FinlandHeart and Lung Center, Helsinki University Central Hospital, and Helsinki University, Helsinki, FinlandDepartment of Neurology, Helsinki University Hospital and University of Helsinki, Helsinki, FinlandDepartment of Oral and Maxillofacial Diseases, University of Helsinki, Helsinki, FinlandDepartment of Oral and Maxillofacial Diseases, University of Helsinki, Helsinki, FinlandBackground Gingivitis, i.e. inflammation of the gums, is often induced by dental plaque. However, its exact link to the oral microbiota remains unclear.Methods In a case-control study involving 120 participants, comprising 60 cases and 60 controls (mean age (SD) 36.6 (7.6) years; 50% males), nested within a prospective multicentre cohort study, we examined the oral microbiome composition of gingivitis patients and their controls using shotgun metagenomic sequencing of saliva samples. Participants underwent clinical and radiographic oral health examinations, including bleeding on probing (BOP), at six tooth sites. BOP ≥33% was considered ‘generalized gingivitis/initial periodontitis’(GG/IP), and BOP <33% as ‘healthy and localized gingivitis’(H/LG). Functional potential was inferred using HUMANn3.Results GG/IP exhibited an increase in the abundance of Actinomyces, Porphyromonas, Aggregatibacter, Corynebacterium, Olsenella, and Treponema, whereas H/LG exhibited an increased abundance of Candidatus Nanosynbacter. Nineteen bacterial species and four microbial functional profiles, including L-methionine, glycogen, and inosine-5’-phosphate biosynthesis, were associated with GG/IP. Constructing models with multiple markers resulted in a strong predictive value for GG/IP, with an area under the curve (ROC) of 0.907 (95% CI: 0.848-0.966).Conclusion We observed distinct differences in the oral microbiome between the GG/IP and H/LG groups, indicating similar yet unique microbial profiles and emphasizing their potential role in progression of periodontal diseases.https://www.tandfonline.com/doi/10.1080/20002297.2024.2330867Metagenomicsoral microbiomeperiodontal diseasechronic periodontitissalivabiomarker
spellingShingle Muhammed Manzoor
Jaakko Leskelä
Milla Pietiäinen
Nicolas Martinez-Majander
Eija Könönen
Teemu Niiranen
Leo Lahti
Juha Sinisalo
Jukka Putaala
Pirkko J. Pussinen
Susanna Paju
Shotgun metagenomic analysis of the oral microbiome in gingivitis: a nested case-control study
Journal of Oral Microbiology
Metagenomics
oral microbiome
periodontal disease
chronic periodontitis
saliva
biomarker
title Shotgun metagenomic analysis of the oral microbiome in gingivitis: a nested case-control study
title_full Shotgun metagenomic analysis of the oral microbiome in gingivitis: a nested case-control study
title_fullStr Shotgun metagenomic analysis of the oral microbiome in gingivitis: a nested case-control study
title_full_unstemmed Shotgun metagenomic analysis of the oral microbiome in gingivitis: a nested case-control study
title_short Shotgun metagenomic analysis of the oral microbiome in gingivitis: a nested case-control study
title_sort shotgun metagenomic analysis of the oral microbiome in gingivitis a nested case control study
topic Metagenomics
oral microbiome
periodontal disease
chronic periodontitis
saliva
biomarker
url https://www.tandfonline.com/doi/10.1080/20002297.2024.2330867
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