Oral bacterial diversity is inversely correlated with mucosal inflammation

Karolin Hijazi; Roderick W. Morrison; Indrani Mukhopadhya; Brennan Martin; Matthew Gemmell; Sophie Shaw; Francesco Santoro

doi:10.1111/odi.13420

Oral bacterial diversity is inversely correlated with mucosal inflammation

Karolin Hijazi^*, Roderick W. Morrison, Indrani Mukhopadhya, Brennan Martin, Matthew Gemmell, Sophie Shaw, Francesco Santoro

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

23 Citations (Scopus)

5 Downloads (Pure)

Abstract

Objective
We investigated the relationship amongst the oral mucosal bacterial community, clinical severity and inflammatory markers in the two most common immune‐mediated oral mucosal diseases, namely recurrent aphthous stomatitis (RAS) and oral lichen planus (LP).

Methods
Patients with RAS (n=15), LP (n=18) and healthy controls (n=13) were recruited using criteria to reduce the effect of factors that influence the microbiota structure independently of oral mucosal disease. Clinical severity was quantified using validated scoring methods. DNA was extracted from oral mucosal swabs for 16S rRNA gene high‐throughput sequencing. Salivary cytokines were measured using Cytometric Bead Assays. Correlation studies were conducted amongst microbial diversity, clinical scores and cytokine concentrations.

Results
We observed a significant reduction of bacterial diversity in LP and RAS patients compared to controls (P=0.021 and 0.044, respectively). Reduced bacterial diversity in LP and RAS correlated with increased clinical scores of the two conditions (⍴= ‐0.551 to ‐0.714). A negative correlation was observed between microbial diversity and salivary interferon‐γ, interleukin‐17A, interleukin‐1β (⍴= ‐0.325 to ‐0.449).

Conclusions
This study reports reduced oral microbial diversity in the context of increased mucosal inflammation and supports the role for microbial diversity as a marker or contributor to oral mucosal inflammatory disease activity and development.

Original language	English
Pages (from-to)	1566-1575
Number of pages	10
Journal	Oral Diseases
Volume	26
Issue number	7
Early online date	3 Jun 2020
DOIs	https://doi.org/10.1111/odi.13420
Publication status	Published - Oct 2020

Bibliographical note

Open Access via the Wiley Jisc Agreement
Acknowledgements: This work was funded by Tenovus Scotland (Registered Charity Number: SC009675, Glasgow, UK) and the NHS Grampian Endowment Fund. We thank all patients and healthy volunteers for contributing to this study, clinical and administrative staff for valuable assistance in patient recruitment.

Keywords

oral ulcer
oral mucosa
lichen planus
microbiota
cytokines
saliva
BIOFILMS
DISEASE
MICROBIAL COMMUNITY
T-CELLS
SALIVA

Access to Document

10.1111/odi.13420Licence: CC BY

Hijazi_etal_odi_oralbacteri_a_VOR
© 2020 The Authors. Oral Diseases published by John Wiley & Sons Ltd This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. https://creativecommons.org/licenses/by/4.0/
Final published version, 1.18 MBLicence: CC BY

Cite this

@article{feb5c79ba0f645b298ac143f5e490fcc,

title = "Oral bacterial diversity is inversely correlated with mucosal inflammation",

abstract = "ObjectiveWe investigated the relationship amongst the oral mucosal bacterial community, clinical severity and inflammatory markers in the two most common immune‐mediated oral mucosal diseases, namely recurrent aphthous stomatitis (RAS) and oral lichen planus (LP).MethodsPatients with RAS (n=15), LP (n=18) and healthy controls (n=13) were recruited using criteria to reduce the effect of factors that influence the microbiota structure independently of oral mucosal disease. Clinical severity was quantified using validated scoring methods. DNA was extracted from oral mucosal swabs for 16S rRNA gene high‐throughput sequencing. Salivary cytokines were measured using Cytometric Bead Assays. Correlation studies were conducted amongst microbial diversity, clinical scores and cytokine concentrations.ResultsWe observed a significant reduction of bacterial diversity in LP and RAS patients compared to controls (P=0.021 and 0.044, respectively). Reduced bacterial diversity in LP and RAS correlated with increased clinical scores of the two conditions (⍴= ‐0.551 to ‐0.714). A negative correlation was observed between microbial diversity and salivary interferon‐γ, interleukin‐17A, interleukin‐1β (⍴= ‐0.325 to ‐0.449).ConclusionsThis study reports reduced oral microbial diversity in the context of increased mucosal inflammation and supports the role for microbial diversity as a marker or contributor to oral mucosal inflammatory disease activity and development.",

keywords = "oral ulcer, oral mucosa, lichen planus, microbiota, cytokines, saliva, BIOFILMS, DISEASE, MICROBIAL COMMUNITY, T-CELLS, SALIVA",

author = "Karolin Hijazi and Morrison, {Roderick W.} and Indrani Mukhopadhya and Brennan Martin and Matthew Gemmell and Sophie Shaw and Francesco Santoro",

note = "Open Access via the Wiley Jisc Agreement Acknowledgements: This work was funded by Tenovus Scotland (Registered Charity Number: SC009675, Glasgow, UK) and the NHS Grampian Endowment Fund. We thank all patients and healthy volunteers for contributing to this study, clinical and administrative staff for valuable assistance in patient recruitment.",

year = "2020",

month = oct,

doi = "10.1111/odi.13420",

language = "English",

volume = "26",

pages = "1566--1575",

journal = "Oral Diseases",

issn = "1354-523X",

publisher = "Wiley-Blackwell",

number = "7",

}

TY - JOUR

T1 - Oral bacterial diversity is inversely correlated with mucosal inflammation

AU - Hijazi, Karolin

AU - Morrison, Roderick W.

AU - Mukhopadhya, Indrani

AU - Martin, Brennan

AU - Gemmell, Matthew

AU - Shaw, Sophie

AU - Santoro, Francesco

N1 - Open Access via the Wiley Jisc Agreement Acknowledgements: This work was funded by Tenovus Scotland (Registered Charity Number: SC009675, Glasgow, UK) and the NHS Grampian Endowment Fund. We thank all patients and healthy volunteers for contributing to this study, clinical and administrative staff for valuable assistance in patient recruitment.

PY - 2020/10

Y1 - 2020/10

N2 - ObjectiveWe investigated the relationship amongst the oral mucosal bacterial community, clinical severity and inflammatory markers in the two most common immune‐mediated oral mucosal diseases, namely recurrent aphthous stomatitis (RAS) and oral lichen planus (LP).MethodsPatients with RAS (n=15), LP (n=18) and healthy controls (n=13) were recruited using criteria to reduce the effect of factors that influence the microbiota structure independently of oral mucosal disease. Clinical severity was quantified using validated scoring methods. DNA was extracted from oral mucosal swabs for 16S rRNA gene high‐throughput sequencing. Salivary cytokines were measured using Cytometric Bead Assays. Correlation studies were conducted amongst microbial diversity, clinical scores and cytokine concentrations.ResultsWe observed a significant reduction of bacterial diversity in LP and RAS patients compared to controls (P=0.021 and 0.044, respectively). Reduced bacterial diversity in LP and RAS correlated with increased clinical scores of the two conditions (⍴= ‐0.551 to ‐0.714). A negative correlation was observed between microbial diversity and salivary interferon‐γ, interleukin‐17A, interleukin‐1β (⍴= ‐0.325 to ‐0.449).ConclusionsThis study reports reduced oral microbial diversity in the context of increased mucosal inflammation and supports the role for microbial diversity as a marker or contributor to oral mucosal inflammatory disease activity and development.

AB - ObjectiveWe investigated the relationship amongst the oral mucosal bacterial community, clinical severity and inflammatory markers in the two most common immune‐mediated oral mucosal diseases, namely recurrent aphthous stomatitis (RAS) and oral lichen planus (LP).MethodsPatients with RAS (n=15), LP (n=18) and healthy controls (n=13) were recruited using criteria to reduce the effect of factors that influence the microbiota structure independently of oral mucosal disease. Clinical severity was quantified using validated scoring methods. DNA was extracted from oral mucosal swabs for 16S rRNA gene high‐throughput sequencing. Salivary cytokines were measured using Cytometric Bead Assays. Correlation studies were conducted amongst microbial diversity, clinical scores and cytokine concentrations.ResultsWe observed a significant reduction of bacterial diversity in LP and RAS patients compared to controls (P=0.021 and 0.044, respectively). Reduced bacterial diversity in LP and RAS correlated with increased clinical scores of the two conditions (⍴= ‐0.551 to ‐0.714). A negative correlation was observed between microbial diversity and salivary interferon‐γ, interleukin‐17A, interleukin‐1β (⍴= ‐0.325 to ‐0.449).ConclusionsThis study reports reduced oral microbial diversity in the context of increased mucosal inflammation and supports the role for microbial diversity as a marker or contributor to oral mucosal inflammatory disease activity and development.

KW - oral ulcer

KW - oral mucosa

KW - lichen planus

KW - microbiota

KW - cytokines

KW - saliva

KW - BIOFILMS

KW - DISEASE

KW - MICROBIAL COMMUNITY

KW - T-CELLS

KW - SALIVA

UR - http://www.scopus.com/inward/record.url?scp=85085744540&partnerID=8YFLogxK

U2 - 10.1111/odi.13420

DO - 10.1111/odi.13420

M3 - Article

C2 - 32419230

SN - 1354-523X

VL - 26

SP - 1566

EP - 1575

JO - Oral Diseases

JF - Oral Diseases

IS - 7

ER -

Oral bacterial diversity is inversely correlated with mucosal inflammation

Abstract

Bibliographical note

Keywords

Access to Document

Other files and links

Fingerprint

Karolin Hijazi

Centre for Genome-Enabled Biology and Medicine

Cite this

Oral bacterial diversity is inversely correlated with mucosal inflammation

Abstract

Bibliographical note

Keywords

Access to Document

Other files and links

Fingerprint

Profiles

Karolin Hijazi

Equipment

Centre for Genome-Enabled Biology and Medicine

Cite this