Exploring oral microbiome in oral squamous cell carcinoma across environment-associated sample types

Study information

Reviewed Marked as Reviewed by Svetlana up on 2025-4-1

study design

meta-analysis

Citation

PMID PubMed identifier for scientific articles.

40013780

DOI Digital object identifier for electronic documents.

10.1128/spectrum.00852-24

URI

Authors

Wang Z, Chen Y, Li H, Yue Y, Yu H

Journal

Microbiology spectrum

Year

2025

Keywords:

16S rRNA, meta-analysis, oncogenesis, oral microbiome, oral squamous cell carcinoma

The relationship between the oral microbiome and oral squamous cell carcinoma (OSCC) has been extensively investigated. Nonetheless, most previous studies were single-center, resulting in the absence of systematic evaluations. To address this gap, we performed a comprehensive meta-analysis on 1,255 samples from OSCC-related 16S rRNA gene data sets, representing a diverse range of OSCC phenotypes. It is recognized that the progression of cancer is related to the alterations in the microbiome among different phenotypes. Our findings revealed distinct microbiome characteristics among different sample types, with Biopsy (Bios) and Swab samples exhibiting significant differences between phenotypes. In Bios samples, the microbiomes of the Cancer group and the normal tissue adjacent to the tumor (NAT) group display a higher similarity, while both differ from the microbiome of the Fibroepithelial polyp (FEP) group. Moreover, the identified differential genera and pathways corresponded with these observations. We developed a diagnostic model using the random forest algorithm on Swab samples, achieving an area under the receiver operating characteristic curve (AUC) of 0.918. Importantly, this model exhibited considerable effectiveness (AUC = 0.849) when applied to another sequencing platform. Taken together, our study provides a comprehensive overview of the oral microbiome during various OSCC progression stages, potentially enhancing early detection and treatment.IMPORTANCEThis study answers key questions regarding the universal microbial characteristics and comprehensive oral microbiome dynamics during oral squamous cell carcinoma (OSCC) progression. By integrating multiple data sets, we examine the following critical aspects: (1) Do different sample types harbor distinct microbial communities within the oral cavity? (2) Which sample types offer greater potential for investigating OSCC progression? (3) How are the oral microbiomes of the Cancer group, normal tissue adjacent to the tumor group, and Fibroepithelial polyp group related, and what is their potential association with OSCC development? (4) Can a diagnostic model based on microbial signatures effectively distinguish between Cancer and Health groups using Swab samples?

Experiment 1

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Reviewed Marked as Reviewed by Svetlana up on 2025-4-1

Curated date: 2025/03/23

Curator: Francisca

Revision editor(s): Francisca, Joiejoie, KateRasheed

Subjects

Location of subjects: China; India; Saudi Arabia; Sri Lanka; Yemen

Host species Species from which microbiome was sampled. Contact us to have more species added.: Homo sapiens

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology: Oral cavity Bucca,Buccal cavity,Cavity of mouth,Oral cavity,oral cavity

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology: Oral squamous cell carcinoma mouth scc,mouth squamous cell carcinoma,OCSC,oral cavity scc,oral cavity squamous cell cancer,oral cavity squamous cell carcinoma,oral squamous cell carcinoma,scc of mouth,scc of oral cavity,scc of the mouth,scc of the oral cavity,squamous cell carcinoma of mouth,squamous cell carcinoma of oral cavity,squamous cell carcinoma of the mouth,squamous cell carcinoma of the oral cavity,Oral squamous cell carcinoma

Group 0 name Corresponds to the control (unexposed) group for case-control studies: NAT (Normal Adjacent Tissue)

Group 1 name Corresponds to the case (exposed) group for case-control studies: Cancer group

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group: This group consists of samples from individuals diagnosed with oral squamous cell carcinoma (OSCC)

Group 0 sample size Number of subjects in the control (unexposed) group: 78

Group 1 sample size Number of subjects in the case (exposed) group: 166

Lab analysis

Sequencing type: 16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene: V4

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance: Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).: arcsine square-root

Statistical test: MaAsLin2

Significance threshold p-value or FDR threshold used for differential abundance testing (if any): 0.05

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?: Yes

Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment: geographic area

Alpha Diversity

Pielou Quantifies how equal the community is numerically: decreased

Shannon Estimator of species richness and species evenness: more weight on species richness: decreased

Richness Number of species: decreased

Signature 1

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Curated date: 2025/03/29

Curator: Francisca

Revision editor(s): Francisca, Joiejoie

Source: Fig. 4E

Description: Relative abundance of significantly different bacterial genera between pairwise comparisons of the phenotypes in Bios samples.

Abundance in Group 1: decreased abundance in Cancer group

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Anoxybacillus
Bacillus
Bacteroides
Blautia
Clostridium
Collinsella
Granulicatella
Megasphaera
Neisseriaceae
Serratia
Streptococcus
Veillonella
TM7-3TM7-3

Revision editor(s): Francisca, Joiejoie

Experiment 2

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Curated date: 2025/03/28

Curator: Francisca

Revision editor(s): Francisca, Joiejoie, KateRasheed

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies: FEP (Fibroepithelial polyp)

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group: This group refers to a benign oral mucosal lesion characterized by fibrous connective tissue overgrowth.

Group 1 sample size Number of subjects in the case (exposed) group: 26

Alpha Diversity

Pielou Quantifies how equal the community is numerically: decreased

Shannon Estimator of species richness and species evenness: more weight on species richness: decreased

Richness Number of species: decreased

Signature 1

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Curated date: 2025/03/29

Curator: Francisca

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Source: Fig. 4E

Description: Relative abundance of significantly different bacterial genera between pairwise comparisons of the phenotypes in Bios samples.

Abundance in Group 1: increased abundance in FEP (Fibroepithelial polyp)

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Streptococcus

Revision editor(s): Francisca, Joiejoie

Signature 2

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Curated date: 2025/03/29

Curator: Francisca

Revision editor(s): Francisca, Joiejoie

Source: Fig. 4E

Description: Relative abundance of significantly different bacterial genera between pairwise comparisons of the phenotypes in Bios samples.

Abundance in Group 1: decreased abundance in FEP (Fibroepithelial polyp)

NCBI	Quality Control	Links
Dialister
Gemella
Geodermatophilaceae
Johnsonella
Oribacterium
Phascolarctobacterium
Pseudomonadaceae
Staphylococcus

Revision editor(s): Francisca, Joiejoie

Experiment 3

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Your review change was submittedDuplicate this Experiment Add a new Signature

Reviewed Marked as Reviewed by Svetlana up on 2025-4-1

Curated date: 2025/03/28

Curator: Francisca

Revision editor(s): Francisca, Joiejoie, KateRasheed

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies: FEP

Group 1 name Corresponds to the case (exposed) group for case-control studies: Cancer

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group: This group consists of samples from individuals diagnosed with oral squamous cell carcinoma (OSCC)