Metagenomic characterization of oral microbiome signatures to predict upper gastrointestinal and pancreaticobiliary cancers: a case–control study
Abstract Background This study investigated the oral microbiome signatures associated with upper gastrointestinal (GI) and pancreaticobiliary cancers. Methods Saliva samples from cancer patients and age- and sex-matched healthy controls were analyzed using 16S rRNA-targeted sequencing, followed by c...
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BMC
2025-01-01
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| Series: | Journal of Translational Medicine |
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| Online Access: | https://doi.org/10.1186/s12967-024-05989-9 |
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| author | Sujin Oh Jaihwan Kim Cheol Min Shin Hyo-Jung Lee Hye Seung Lee Kyoung Un Park |
| author_facet | Sujin Oh Jaihwan Kim Cheol Min Shin Hyo-Jung Lee Hye Seung Lee Kyoung Un Park |
| author_sort | Sujin Oh |
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| description | Abstract Background This study investigated the oral microbiome signatures associated with upper gastrointestinal (GI) and pancreaticobiliary cancers. Methods Saliva samples from cancer patients and age- and sex-matched healthy controls were analyzed using 16S rRNA-targeted sequencing, followed by comprehensive bioinformatics analysis. Results Significant dissimilarities in microbial composition were observed between cancer patients and controls across esophageal cancer (EC), gastric cancer (GC), biliary tract cancer (BC), and pancreatic cancer (PC) groups (R2 = 0.067, = 0.075, = 0.068, and = 0.044; p = 0.001, = 0.001, = 0.002, and = 0.004, respectively). Additionally, the oral microbiome composition significantly differed by the four cancer sites (p = 0.001 for EC vs. GC, EC vs. BC, EC vs. PC, GC vs. BC, and GC vs. PC; p = 0.013 for BC vs. PC). We built oral metagenomic classifiers to predict cancer and selected specific microbial taxa with diagnostic properties. For EC, the classifier differentiated cancer patients and controls with good accuracy (area under the curve [AUC] = 0.791) and included three genera: Akkermansia, Escherichia-Shigella, and Subdoligranulum. For GC, the classifier exhibited high discriminative power (AUC = 0.961); it included five genera (Escherichia-Shigella, Gemella, Holdemanella, Actinomyces, and Stomatobaculum) and three species (Eubacterium sp. oral clone EI074, Ruminococcus sp. Marseille-P328, and Leptotrichia wadei F0279). However, microbial taxa with diagnostic features for BC and PC were not identified. Conclusions These findings suggested that the oral microbiome composition may serve as an indicator of tumorigenesis in upper GI and pancreaticobiliary cancers. The development of oral metagenomic classifiers for EC and GC demonstrates the potential value of microbial biomarkers in cancer screening. |
| format | Article |
| id | doaj-art-96e53ac4f5d041f1ba7b52c5169d1b95 |
| institution | Kabale University |
| issn | 1479-5876 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Journal of Translational Medicine |
| spelling | doaj-art-96e53ac4f5d041f1ba7b52c5169d1b952025-01-12T12:37:36ZengBMCJournal of Translational Medicine1479-58762025-01-0123111710.1186/s12967-024-05989-9Metagenomic characterization of oral microbiome signatures to predict upper gastrointestinal and pancreaticobiliary cancers: a case–control studySujin Oh0Jaihwan Kim1Cheol Min Shin2Hyo-Jung Lee3Hye Seung Lee4Kyoung Un Park5Department of Laboratory Medicine, Seoul National University College of MedicineDepartment of Internal Medicine, Seoul National University Bundang HospitalDepartment of Internal Medicine, Seoul National University Bundang HospitalDepartment of Periodontology, Section of Dentistry, Seoul National University Bundang HospitalDepartment of Pathology, Seoul National University College of MedicineDepartment of Laboratory Medicine, Seoul National University College of MedicineAbstract Background This study investigated the oral microbiome signatures associated with upper gastrointestinal (GI) and pancreaticobiliary cancers. Methods Saliva samples from cancer patients and age- and sex-matched healthy controls were analyzed using 16S rRNA-targeted sequencing, followed by comprehensive bioinformatics analysis. Results Significant dissimilarities in microbial composition were observed between cancer patients and controls across esophageal cancer (EC), gastric cancer (GC), biliary tract cancer (BC), and pancreatic cancer (PC) groups (R2 = 0.067, = 0.075, = 0.068, and = 0.044; p = 0.001, = 0.001, = 0.002, and = 0.004, respectively). Additionally, the oral microbiome composition significantly differed by the four cancer sites (p = 0.001 for EC vs. GC, EC vs. BC, EC vs. PC, GC vs. BC, and GC vs. PC; p = 0.013 for BC vs. PC). We built oral metagenomic classifiers to predict cancer and selected specific microbial taxa with diagnostic properties. For EC, the classifier differentiated cancer patients and controls with good accuracy (area under the curve [AUC] = 0.791) and included three genera: Akkermansia, Escherichia-Shigella, and Subdoligranulum. For GC, the classifier exhibited high discriminative power (AUC = 0.961); it included five genera (Escherichia-Shigella, Gemella, Holdemanella, Actinomyces, and Stomatobaculum) and three species (Eubacterium sp. oral clone EI074, Ruminococcus sp. Marseille-P328, and Leptotrichia wadei F0279). However, microbial taxa with diagnostic features for BC and PC were not identified. Conclusions These findings suggested that the oral microbiome composition may serve as an indicator of tumorigenesis in upper GI and pancreaticobiliary cancers. The development of oral metagenomic classifiers for EC and GC demonstrates the potential value of microbial biomarkers in cancer screening.https://doi.org/10.1186/s12967-024-05989-9Oral microbiomeEsophageal cancerGastric cancerBiliary tract cancerPancreatic cancerMicrobial signatures |
| spellingShingle | Sujin Oh Jaihwan Kim Cheol Min Shin Hyo-Jung Lee Hye Seung Lee Kyoung Un Park Metagenomic characterization of oral microbiome signatures to predict upper gastrointestinal and pancreaticobiliary cancers: a case–control study Journal of Translational Medicine Oral microbiome Esophageal cancer Gastric cancer Biliary tract cancer Pancreatic cancer Microbial signatures |
| title | Metagenomic characterization of oral microbiome signatures to predict upper gastrointestinal and pancreaticobiliary cancers: a case–control study |
| title_full | Metagenomic characterization of oral microbiome signatures to predict upper gastrointestinal and pancreaticobiliary cancers: a case–control study |
| title_fullStr | Metagenomic characterization of oral microbiome signatures to predict upper gastrointestinal and pancreaticobiliary cancers: a case–control study |
| title_full_unstemmed | Metagenomic characterization of oral microbiome signatures to predict upper gastrointestinal and pancreaticobiliary cancers: a case–control study |
| title_short | Metagenomic characterization of oral microbiome signatures to predict upper gastrointestinal and pancreaticobiliary cancers: a case–control study |
| title_sort | metagenomic characterization of oral microbiome signatures to predict upper gastrointestinal and pancreaticobiliary cancers a case control study |
| topic | Oral microbiome Esophageal cancer Gastric cancer Biliary tract cancer Pancreatic cancer Microbial signatures |
| url | https://doi.org/10.1186/s12967-024-05989-9 |
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