Characteristics of the oral and gastric microbiome in patients with early-stage intramucosal esophageal squamous cell carcinoma

Study information

Needs review

study design

case-control

Citation

PMID PubMed identifier for scientific articles.

38491387

DOI Digital object identifier for electronic documents.

10.1186/s12866-024-03233-4

URI

Authors

Chen H, Jiang X, Zhu F, Yang R, Yu X, Zhou X, Tang N

Journal

BMC microbiology

Year

2024

Keywords:

Amplicon sequencing analysis, Early esophageal cancer, Gastric microbiome, Intramucosal esophageal squamous carcinoma, Oral microbiome

BACKGROUND: Oral microbiome dysbacteriosis has been reported to be associated with the pathogenesis of advanced esophageal cancer. However, few studies investigated the potential role of oral and gastric microbiota in early-stage intramucosal esophageal squamous carcinoma (EIESC). METHOD: A total of 104 samples were collected from 31 patients with EIESC and 21 healthy controls. The compositions of oral and gastric microbiota were analyzed using 16 S rRNA V3-V4 amplicon sequencing. Linear discriminant analysis effect size (LEfSe) analysis was performed to assess taxonomic differences between groups. The correlation between oral microbiota and clinicopathological factors was evaluated using Spearman correlation analysis. Additionally, co-occurrence networks were established and random forest models were utilized to identify significant microbial biomarkers for distinguishing between the EIESC and control groups. RESULTS: A total of 292 oral genera and 223 species were identified in both EIESC and healthy controls. Six oral genera were remarkably enriched in EIESC groups, including the genera Porphyromonas, Shigella, Subdoligranulum, Leptotrichia, Paludibacter, and Odoribacter. LEfSe analysis identified genera Porphyromonas and Leptotrichia with LDA scores > 3. In the random forest model, Porphyromonas endodontalis ranked the top microbial biomarker to differentiate EIESC from controls. The elimination rate of Porphyromonas endodontalis from the oral cavity to the stomach was also dramatically decreased in the EIESC group than controls. In the microbial co-occurrence network, Porphyromonas endodontalis was positively correlated with Prevotella tannerae and Prevotella intermedia and was negatively correlated with Veillonella dispar. CONCLUSION: Our study potentially indicates that the dysbacteriosis of both the oral and gastric microbiome was associated with EIESC. Larger scale studies and experimental animal models are urgently needed to confirm the possible role of microbial dysbacteriosis in the pathogenesis of EIESC. (Chinese Clinical Trial Registry Center, ChiCTR2200063464, Registered 07 September 2022, https://www.chictr.org.cn/showproj.html?proj=178563).

Experiment 1

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Curated date: 2024/03/19

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Subjects

Location of subjects: China

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: Saliva Sailva normalis,Saliva atomaris,Saliva molecularis,Salivary gland secretion,Saliva,saliva

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology: Esophageal squamous cell carcinoma ESCC,esophageal epidermoid carcinoma,esophageal scc,esophageal squamous cell cancer,esophageal squamous cell carcinoma,esophagus scc,esophagus squamous cell carcinoma,scc of esophagus,scc of the esophagus,squamous cell car. - esophagus,squamous cell carcinoma of esophagus,squamous cell carcinoma of the esophagus,Esophageal squamous cell carcinoma

Group 0 name Corresponds to the control (unexposed) group for case-control studies: NC_oral - No carcinoma.

Group 1 name Corresponds to the case (exposed) group for case-control studies: EIESC_oral - Early-stage intramucosal esophageal squamous carcinoma.

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group: Saliva was collected from patients diagnosed with early-stage intramucosal esophageal squamous carcinoma (EIESC).

Group 0 sample size Number of subjects in the control (unexposed) group: 21

Group 1 sample size Number of subjects in the case (exposed) group: 31

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any): Patients who have used antibiotics 4 weeks before admission.

Lab analysis

Sequencing type: 16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene: V3-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).: relative abundances

Statistical test: LEfSe

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

LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool: 2

Alpha Diversity

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

Chao1 Abundance-based estimator of species richness: unchanged

Simpson Estimator of species richness and species evenness: more weight on species evenness: unchanged

Signature 1

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Curated date: 2024/03/20

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Source: Fig. 5A

Description: LEfSe analysis. Plot of LDA Effect Size. The length of the bar column represents the LDA score. The figure shows the oral microbial taxa with significant differences between the EIESC (orange) and Control (green) (LDA score>2)

Abundance in Group 1: increased abundance in EIESC_oral - Early-stage intramucosal esophageal squamous carcinoma.

NCBI	Quality Control	Links
Fusobacteriales
Fusobacteriia
Fusobacteriota
Leptotrichia
Leptotrichiaceae
Parvimonas
Porphyromonadaceae
Porphyromonas
Pyramidobacter

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Source: Fig. 5A

Description: LEfSe analysis. Plot of LDA Effect Size. The length of the bar column represents the LDA score. The figure shows the oral microbial taxa with significant differences between the EIESC (orange) and Control (green) (LDA score > 2).

Abundance in Group 1: decreased abundance in EIESC_oral - Early-stage intramucosal esophageal squamous carcinoma.

NCBI	Quality Control	Links
Campylobacter
Campylobacteraceae
Campylobacterales
Clostridium
Epsilonproteobacteria
Gemmatimonadales
Lysobacter
Promicromonosporaceae
Thermomicrobia
Gemm_5Gemm_5
JG30_KF_CM45JG30_KF_CM45

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Experiment 2

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Differences from previous experiment shown

Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology: Mucosa of body of stomach Body of stomach mucosa,Body of stomach mucosa of organ,Body of stomach mucous membrane,Body of stomach organ mucosa,Corpus gastricum (ventriculare) mucosa,Corpus gastricum (ventriculare) mucosa of organ,Corpus gastricum (ventriculare) mucous membrane,Corpus gastricum (ventriculare) organ mucosa,Gastric body mucosa,Gastric body mucosa of organ,Gastric body mucous membrane,Gastric body organ mucosa,Mucosa of corpus gastricum (ventriculare),Mucosa of gastric body,Mucosa of organ of body of stomach,Mucosa of organ of corpus gastricum (ventriculare),Mucosa of organ of gastric body,Mucosa of organ of stomach body,Mucosa of stomach body,Mucous membrane of body of stomach,Mucous membrane of corpus gastricum (ventriculare),Mucous membrane of gastric body,Mucous membrane of stomach body,Organ mucosa of body of stomach,Organ mucosa of corpus gastricum (ventriculare),Organ mucosa of gastric body,Organ mucosa of stomach body,Stomach body mucosa,Stomach body mucosa of organ,Stomach body mucous membrane,Stomach body organ mucosa,Mucosa of body of stomach,mucosa of body of stomach

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

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

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group: Gastric biopsy samples were obtained from patients diagnosed with early-stage intramucosal esophageal squamous carcinoma (EIESC).