Characteristics of Microbial Distribution in Different Oral Niches of Oral Squamous Cell Carcinoma

Oral squamous cell carcinoma (OSCC), one of the most common malignant tumors of the head and neck, is closely associated with the presence of oral microbes. However, the microbiomes of different oral niches in OSCC patients and their association with OSCC have not been adequately characterized. In t...

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Main Authors: Fujiao Nie, Lihua Wang, Yingying Huang, Pishan Yang, Pizhang Gong, Qiang Feng, Chengzhe Yang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2022.905653/full
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author Fujiao Nie
Fujiao Nie
Lihua Wang
Lihua Wang
Yingying Huang
Yingying Huang
Pishan Yang
Pishan Yang
Pizhang Gong
Pizhang Gong
Qiang Feng
Qiang Feng
Chengzhe Yang
Chengzhe Yang
author_facet Fujiao Nie
Fujiao Nie
Lihua Wang
Lihua Wang
Yingying Huang
Yingying Huang
Pishan Yang
Pishan Yang
Pizhang Gong
Pizhang Gong
Qiang Feng
Qiang Feng
Chengzhe Yang
Chengzhe Yang
author_sort Fujiao Nie
collection DOAJ
description Oral squamous cell carcinoma (OSCC), one of the most common malignant tumors of the head and neck, is closely associated with the presence of oral microbes. However, the microbiomes of different oral niches in OSCC patients and their association with OSCC have not been adequately characterized. In this study, 305 samples were collected from 65 OSCC patients, including tumor tissue, adjacent normal tissue (paracancerous tissue), cancer surface tissue, anatomically matched contralateral normal mucosa, saliva, and tongue coat. 16S ribosomal DNA (16S rDNA) sequencing was used to compare the microbial composition, distribution, and co-occurrence network of different oral niches. The association between the microbiome and the clinical features of OSCC was also characterized. The oral microbiome of OSCC patients showed a regular ecological distribution. Tumor and paracancerous tissues were more microbially diverse than other oral niches. Cancer surface, contralateral normal mucosa, saliva, and tongue coat showed similar microbial compositions, especially the contralateral normal mucosa and saliva. Periodontitis-associated bacteria of the genera Fusobacterium, Prevotella, Porphyromonas, Campylobacter, and Aggregatibacter, and anaerobic bacteria were enriched in tumor samples. The microbiome was highly correlated with tumor clinicopathological features, with several genera (Lautropia, Asteroleplasma, Parvimonas, Peptostreptococcus, Pyramidobacter, Roseburia, and Propionibacterium) demonstrating a relatively high diagnostic power for OSCC metastasis, potentially providing an indicator for the development of OSCC.
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spelling doaj.art-107964a0a6e94d66ae6a20a1b38ceb182022-12-22T01:35:52ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882022-08-011210.3389/fcimb.2022.905653905653Characteristics of Microbial Distribution in Different Oral Niches of Oral Squamous Cell CarcinomaFujiao Nie0Fujiao Nie1Lihua Wang2Lihua Wang3Yingying Huang4Yingying Huang5Pishan Yang6Pishan Yang7Pizhang Gong8Pizhang Gong9Qiang Feng10Qiang Feng11Chengzhe Yang12Chengzhe Yang13Department of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University, Jinan, ChinaShandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Laboratory for Dental Materials and Oral Tissue Regeneration, Jinan, ChinaDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University, Jinan, ChinaDepartment of Human Microbiome, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University, Jinan, ChinaDepartment of Oral and Maxillofacial Surgery, Qilu Hospital of Shandong University, Jinan, ChinaInstitute of Stomatology, Shandong University, Jinan, ChinaDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University, Jinan, ChinaShandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Laboratory for Dental Materials and Oral Tissue Regeneration, Jinan, ChinaDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University, Jinan, ChinaShandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Laboratory for Dental Materials and Oral Tissue Regeneration, Jinan, ChinaDepartment of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University, Jinan, ChinaDepartment of Human Microbiome, School and Hospital of Stomatology, Cheeloo College of Medicine, Shandong University, Jinan, ChinaDepartment of Oral and Maxillofacial Surgery, Qilu Hospital of Shandong University, Jinan, ChinaInstitute of Stomatology, Shandong University, Jinan, ChinaOral squamous cell carcinoma (OSCC), one of the most common malignant tumors of the head and neck, is closely associated with the presence of oral microbes. However, the microbiomes of different oral niches in OSCC patients and their association with OSCC have not been adequately characterized. In this study, 305 samples were collected from 65 OSCC patients, including tumor tissue, adjacent normal tissue (paracancerous tissue), cancer surface tissue, anatomically matched contralateral normal mucosa, saliva, and tongue coat. 16S ribosomal DNA (16S rDNA) sequencing was used to compare the microbial composition, distribution, and co-occurrence network of different oral niches. The association between the microbiome and the clinical features of OSCC was also characterized. The oral microbiome of OSCC patients showed a regular ecological distribution. Tumor and paracancerous tissues were more microbially diverse than other oral niches. Cancer surface, contralateral normal mucosa, saliva, and tongue coat showed similar microbial compositions, especially the contralateral normal mucosa and saliva. Periodontitis-associated bacteria of the genera Fusobacterium, Prevotella, Porphyromonas, Campylobacter, and Aggregatibacter, and anaerobic bacteria were enriched in tumor samples. The microbiome was highly correlated with tumor clinicopathological features, with several genera (Lautropia, Asteroleplasma, Parvimonas, Peptostreptococcus, Pyramidobacter, Roseburia, and Propionibacterium) demonstrating a relatively high diagnostic power for OSCC metastasis, potentially providing an indicator for the development of OSCC.https://www.frontiersin.org/articles/10.3389/fcimb.2022.905653/fulloral squamous cell carcinomaoral microbiomedistribution characteristicsoral nichesclinicopathological features
spellingShingle Fujiao Nie
Fujiao Nie
Lihua Wang
Lihua Wang
Yingying Huang
Yingying Huang
Pishan Yang
Pishan Yang
Pizhang Gong
Pizhang Gong
Qiang Feng
Qiang Feng
Chengzhe Yang
Chengzhe Yang
Characteristics of Microbial Distribution in Different Oral Niches of Oral Squamous Cell Carcinoma
Frontiers in Cellular and Infection Microbiology
oral squamous cell carcinoma
oral microbiome
distribution characteristics
oral niches
clinicopathological features
title Characteristics of Microbial Distribution in Different Oral Niches of Oral Squamous Cell Carcinoma
title_full Characteristics of Microbial Distribution in Different Oral Niches of Oral Squamous Cell Carcinoma
title_fullStr Characteristics of Microbial Distribution in Different Oral Niches of Oral Squamous Cell Carcinoma
title_full_unstemmed Characteristics of Microbial Distribution in Different Oral Niches of Oral Squamous Cell Carcinoma
title_short Characteristics of Microbial Distribution in Different Oral Niches of Oral Squamous Cell Carcinoma
title_sort characteristics of microbial distribution in different oral niches of oral squamous cell carcinoma
topic oral squamous cell carcinoma
oral microbiome
distribution characteristics
oral niches
clinicopathological features
url https://www.frontiersin.org/articles/10.3389/fcimb.2022.905653/full
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