Clinical relationships between the intratumoral microbiome and risk factors for head and neck cancer

A bioinformatic analysis is a promising approach to understand the relationship between the vast tumor microbiome and cancer development. In the present study, we studied the relationships between the intratumoral microbiome and classical clinical risk factors using bioinformatics analysis of the Ca...

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Main Authors: Masakazu Hamada, Kyoko Nishiyama, Ryota Nomura, Tatsuya Akitomo, Chieko Mitsuhata, Yoshiaki Yura, Kazuhiko Nakano, Michiyo Matsumoto-Nakano, Narikazu Uzawa, Hiroaki Inaba
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Language:English
Published: Elsevier 2024-10-01
Series:Heliyon
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Online Access:http://www.sciencedirect.com/science/article/pii/S2405844024153157
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author Masakazu Hamada
Kyoko Nishiyama
Ryota Nomura
Tatsuya Akitomo
Chieko Mitsuhata
Yoshiaki Yura
Kazuhiko Nakano
Michiyo Matsumoto-Nakano
Narikazu Uzawa
Hiroaki Inaba
author_facet Masakazu Hamada
Kyoko Nishiyama
Ryota Nomura
Tatsuya Akitomo
Chieko Mitsuhata
Yoshiaki Yura
Kazuhiko Nakano
Michiyo Matsumoto-Nakano
Narikazu Uzawa
Hiroaki Inaba
author_sort Masakazu Hamada
collection DOAJ
description A bioinformatic analysis is a promising approach to understand the relationship between the vast tumor microbiome and cancer development. In the present study, we studied the relationships between the intratumoral microbiome and classical clinical risk factors using bioinformatics analysis of the Cancer Genome Atlas (TCGA) and the Cancer Microbiome Atlas (TCMA) datasets. We used TCMA database and investigated the abundance of microbes at the genus level in solid normal tissue (n = 22) and the primary tumors of patients with head and neck squamous cell carcinoma (HNSCC) (n = 154) and identified three major tumor microbiomes, Fusobacterium, Prevotella, and Streptococcus. The tissue level of Fusobacterium was higher in primary tumors than in solid normal tissue. However, univariate and multivariate analyses of these 3 microbes showed no significant effects on patient survival. We then extracted 43, 55, or 59 genes that were differentially expressed between the over and under the median groups for Fusobacterium, Prevotella, or Streptococcus using the criteria of >2.5, >1.5, or >2.0 fold and p < 0.05 in the Mann-Whitney U test. The results of a pathway analysis revealed the association of Fusobacterium- and Streptococcus-related genes with the IL-17 signaling pathway and Staphylococcus aureus infection, while Prevotella-associated pathways were not extracted. A protein-protein interaction analysis revealed a dense network in the order of Fusobacterium, Streptococcus, and Prevotella. An investigation of the relationships between the intratumoral microbiome and classical clinical risk factors showed that high levels of Fusobacterium were associated with a good prognosis in the absence of alcohol consumption and smoking, while high levels of Streptococcus were associated with a poor prognosis in the absence of alcohol consumption. In conclusion, intratumoral Fusobacterium and Streptococcus may affect the prognosis of patients with HNSCC, and their effects on HNSCC are modulated by the impact of drinking and smoking.
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spelling doaj-art-e93cdcbd94e94d90855a63d5c367babd2024-11-12T05:20:17ZengElsevierHeliyon2405-84402024-10-011020e39284Clinical relationships between the intratumoral microbiome and risk factors for head and neck cancerMasakazu Hamada0Kyoko Nishiyama1Ryota Nomura2Tatsuya Akitomo3Chieko Mitsuhata4Yoshiaki Yura5Kazuhiko Nakano6Michiyo Matsumoto-Nakano7Narikazu Uzawa8Hiroaki Inaba9Department of Oral &amp; Maxillofacial Oncology and Surgery, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka, 565-0871, Japan; Corresponding author.Department of Oral &amp; Maxillofacial Oncology and Surgery, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka, 565-0871, JapanDepartment of Pediatric Dentistry, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8553, JapanDepartment of Pediatric Dentistry, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8553, JapanDepartment of Pediatric Dentistry, Graduate School of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8553, JapanDepartment of Oral &amp; Maxillofacial Oncology and Surgery, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka, 565-0871, JapanDepartment of Pediatric Dentistry, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka, 565-0871, JapanDepartment of Pediatric Dentistry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8525, JapanDepartment of Oral &amp; Maxillofacial Oncology and Surgery, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka, 565-0871, JapanDepartment of Pediatric Dentistry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1 Shikata-cho, Kita-ku, Okayama, 700-8525, Japan; Department of Dental Hygiene, Kyoto Koka Woman's College, 38, Kuzuno-cho, Nishikyogoku, Ukyo-ku, Kyoto-shi, 615-0882, JapanA bioinformatic analysis is a promising approach to understand the relationship between the vast tumor microbiome and cancer development. In the present study, we studied the relationships between the intratumoral microbiome and classical clinical risk factors using bioinformatics analysis of the Cancer Genome Atlas (TCGA) and the Cancer Microbiome Atlas (TCMA) datasets. We used TCMA database and investigated the abundance of microbes at the genus level in solid normal tissue (n = 22) and the primary tumors of patients with head and neck squamous cell carcinoma (HNSCC) (n = 154) and identified three major tumor microbiomes, Fusobacterium, Prevotella, and Streptococcus. The tissue level of Fusobacterium was higher in primary tumors than in solid normal tissue. However, univariate and multivariate analyses of these 3 microbes showed no significant effects on patient survival. We then extracted 43, 55, or 59 genes that were differentially expressed between the over and under the median groups for Fusobacterium, Prevotella, or Streptococcus using the criteria of >2.5, >1.5, or >2.0 fold and p < 0.05 in the Mann-Whitney U test. The results of a pathway analysis revealed the association of Fusobacterium- and Streptococcus-related genes with the IL-17 signaling pathway and Staphylococcus aureus infection, while Prevotella-associated pathways were not extracted. A protein-protein interaction analysis revealed a dense network in the order of Fusobacterium, Streptococcus, and Prevotella. An investigation of the relationships between the intratumoral microbiome and classical clinical risk factors showed that high levels of Fusobacterium were associated with a good prognosis in the absence of alcohol consumption and smoking, while high levels of Streptococcus were associated with a poor prognosis in the absence of alcohol consumption. In conclusion, intratumoral Fusobacterium and Streptococcus may affect the prognosis of patients with HNSCC, and their effects on HNSCC are modulated by the impact of drinking and smoking.http://www.sciencedirect.com/science/article/pii/S2405844024153157Intratumor microbiomeOral bacteriaPrevotellaFusobacteriumStreptococcusHead and neck cancer
spellingShingle Masakazu Hamada
Kyoko Nishiyama
Ryota Nomura
Tatsuya Akitomo
Chieko Mitsuhata
Yoshiaki Yura
Kazuhiko Nakano
Michiyo Matsumoto-Nakano
Narikazu Uzawa
Hiroaki Inaba
Clinical relationships between the intratumoral microbiome and risk factors for head and neck cancer
Heliyon
Intratumor microbiome
Oral bacteria
Prevotella
Fusobacterium
Streptococcus
Head and neck cancer
title Clinical relationships between the intratumoral microbiome and risk factors for head and neck cancer
title_full Clinical relationships between the intratumoral microbiome and risk factors for head and neck cancer
title_fullStr Clinical relationships between the intratumoral microbiome and risk factors for head and neck cancer
title_full_unstemmed Clinical relationships between the intratumoral microbiome and risk factors for head and neck cancer
title_short Clinical relationships between the intratumoral microbiome and risk factors for head and neck cancer
title_sort clinical relationships between the intratumoral microbiome and risk factors for head and neck cancer
topic Intratumor microbiome
Oral bacteria
Prevotella
Fusobacterium
Streptococcus
Head and neck cancer
url http://www.sciencedirect.com/science/article/pii/S2405844024153157
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