Carcinogenesis of Male Oral Submucous Fibrosis Alters Salivary Microbiomes

Carcinogenesis of Male Oral Submucous Fibrosis Alters Salivary Microbiomes

Most oral squamous cell carcinoma (OSCC) tumors arise from oral premalignant lesions. Oral submucous fibrosis (OSF), usually occurring in male chewers of betel quid, is a premalignant stromal disease characterized by a high malignant transformation rate and high prevalence. Although a relationship b...

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Bibliographic Details
Published in:Journal of dental research Vol. 100; no. 4; pp. 397 - 405
Main Authors: Chen, M.Y., Chen, J.W., Wu, L.W., Huang, K.C., Chen, J.Y., Wu, W.S., Chiang, W.F., Shih, C.J., Tsai, K.N., Hsieh, W.T., Ho, Y.H., Wong, T.Y., Wu, J.H., Chen, Y.L.
Format: Journal Article
Language:English
Published: Los Angeles, CA SAGE Publications 01-04-2021
SAGE PUBLICATIONS, INC
Subjects:
Artificial Intelligence
Carcinogenesis
Carcinoma, Squamous Cell
Fibrosis
Genetic transformation
Head and Neck Neoplasms
Humans
Male
Malignancy
Methionine
Microbiomes
Microbiota
Mouth Neoplasms
Next-generation sequencing
Oral squamous cell carcinoma
Oral Submucous Fibrosis
Ornithine
Phylogenetics
Phylogeny
Porphyromonas
Prevotella
RNA, Ribosomal, 16S - genetics
rRNA 16S
Species richness
Squamous cell carcinoma
Stochasticity
Tumors
microbiota
saliva
precancerous conditions
machine learning
biomarker
dysbiosis
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Summary:Most oral squamous cell carcinoma (OSCC) tumors arise from oral premalignant lesions. Oral submucous fibrosis (OSF), usually occurring in male chewers of betel quid, is a premalignant stromal disease characterized by a high malignant transformation rate and high prevalence. Although a relationship between the inhabited microbiome and carcinogenesis has been proposed, no detailed information regarding the oral microbiome of patients with OSF exists; the changes of the salivary microbiome during cancer formation remain unclear. This study compared the salivary microbiomes of male patients with OSCC and a predisposing OSF background (OSCC-OSF group) and those with OSF only (OSF group). The results of high-throughput sequencing of the bacterial 16S rRNA gene indicated that OSF-related carcinogenesis and smoking status significantly contributed to phylogenetic composition variations in the salivary microbiome, leading to considerable reductions in species richness and phylogenetic diversity. The microbiome profile of OSF-related malignancy was associated with increased microbial stochastic fluctuation, which dominated the salivary microbiome assembly and caused species co-occurrence network collapse. Artificial intelligence selection algorithms consistently identified 5 key species in the OSCC-OSF group: Porphyromonas catoniae, Prevotella multisaccharivorax, Prevotella sp. HMT-300, Mitsuokella sp. HMT-131, and Treponema sp. HMT-927. Robust accuracy in predicting oral carcinogenesis was obtained with our exploratory and validation data sets. In functional analysis, the microbiome of the OSCC-OSF group had greater potential for S-adenosyl-l-methionine and norspermidine synthesis but lower potential for l-ornithine and pyrimidine deoxyribonucleotide synthesis and formaldehyde metabolism. These findings indicated that the salivary microbiome plays important roles in modulating microbial metabolites during oral carcinogenesis. In conclusion, our results provided new insights into salivary microbiome alterations during the malignant transformation of OSF.
ISSN:0022-0345
1544-0591
DOI:10.1177/0022034520968750