Metagenomic Identification of Microbial Signatures Predicting Pancreatic Cancer From a Multinational Study
Open accessAbstract
BACKGROUND & AIMS: To identify gut and oral metagenomic signatures that accurately predict pancreatic ductal carcinoma (PDAC) and to validate these signatures in independent cohorts. METHODS: We conducted a multinational study and performed shotgun metagenomic analysis of fecal and salivary samples collected from patients with treatment-naïve PDAC and non-PDAC controls in Japan, Spain, and Germany. Taxonomic and functional profiles of the microbiomes were characterized, and metagenomic classifiers to predict PDAC were constructed and validated in external datasets. RESULTS: Comparative metagenomics revealed dysbiosis of both the gut and oral microbiomes and identified 30 gut and 18 oral species significantly associated with PDAC in the Japanese cohort. These microbial signatures achieved high area under the curve values of 0.78 to 0.82. The prediction model trained on the Japanese gut microbiome also had high predictive ability in Spanish and German cohorts, with respective area under the curve values of 0.74 and 0.83, validating its high confidence and versatility for PDAC prediction. Significant enrichments of Streptococcus and Veillonella spp and a depletion of Faecalibacterium prausnitzii were common gut signatures for PDAC in all the 3 cohorts. Prospective follow-up data revealed that patients with certain gut and oral microbial species were at higher risk of PDAC-related mortality. Finally, 58 bacteriophages that could infect microbial species consistently enriched in patients with PDAC across the 3 countries were identified. CONCLUSIONS: Metagenomics targeting the gut and oral microbiomes can provide a powerful source of biomarkers for identifying individuals with PDAC and their prognoses. The identification of shared gut microbial signatures for PDAC in Asian and European cohorts indicates the presence of robust and global gut microbial biomarkers.
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A shared PDAC GOMS showed enrichment of pro-inflammatory Streptococcus and Veillonella spp. and 58 bacteriophages, and depletion of SCFA producers F. prausnitzii, E. rectale, and Ruminococcus bicirculans.
“identified a shared PDAC GOMS in which the pro-inflammatory Streptococcus and Veillonella spp.70 and 58 of their bacteriophages were substantially enriched and SCFA producers (such as F. prausnitzii, E. rectale and Ruminococcus bicirculans) were depleted45”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [45]
Faecal microbiome composition in patients with PDAC differed from individuals without cancer across studies accounting for confounders.
“Across various studies taking into account all known possible cofounding factors relevant to pancreatic ductal adenocarcinoma (PDAC), the faecal microbiome composition in patients with this devastating disease differed from that in individuals without cancer45,54.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [45]
Functional analysis of GOMS in three PDAC cohorts revealed increased biosynthesis of C5 isoprenoid from mevalonate pathway and ADP-L-glycero-D-manno-heptose.
“Functional analysis of GOMS in these three cohorts also revealed a substantial increase in the biosynthesis of C5 isoprenoid from the mevalonate pathway and of ADP-L-glycero-D-manno-heptose in PDAC45.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [45]
Prospective follow-up revealed correlations between PDAC GOMS and PDAC-related mortality; abundance of SCFA producers relative to R. torques, H. parainfluenzae, and N. bacilliformis was associated with prolonged OS.
“Prospective follow-up revealed correlations between the presence of the PDAC GOMS and PDAC-related mortality. An abundance of SCFA producers in the gut relative to that of Ruminococcus torques, Haemophilus parainfluenzae and Neisseria bacilliformis was associated with prolonged overall survival (OS).”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [45]
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- Authors
- Nagata, N., Nishijima, S., Kojima, Y., Hisada, Y., Imbe, K., Miyoshi-Akiyama, T., Suda, W., Kimura, M., Aoki, R., Sekine, K., Ohsugi, M., Miki, K., Osawa, T., Ueki, K., Oka, S., Mizokami, M., Kartal, E., Schmidt, T. S. B., Molina-Montes, E., Estudillo, L., Malats, N., Trebicka, J., Kersting, S., Langheinrich, M., Bork, P., Uemura, N., Itoi, T., & Kawai, T.
- Affiliations
- Tokyo Medical University (JP)
- Waseda University (JP)
- National Center for Global Health and Medicine (JP)
- RIKEN Center for Integrative Medical Sciences (JP)
- Ezaki Glico (Japan) (JP)
- Research Center for Advanced Science and Technology, The University of Tokyo (JP)
- European Molecular Biology Laboratory (DE)
- Spanish National Cancer Research Centre (ES)
- Goethe University Frankfurt (DE)
- Universitätsmedizin Greifswald (DE)
- Corresponding author
- Nagata, Naoyoshi
- Nishijima, Suguru
- ORCID
- Nagata, Naoyoshi
- Nishijima, Suguru
- Kojima, Yasushi
- Hisada, Yuya
- Suda, Wataru
- Kimura, Moto
- Aoki, Ryo
- Sekine, Katsunori
- Ohsugi, Mitsuru
- Osawa, Tsuyoshi
- Ueki, Kohjiro
- Oka, Shinichi
- Mizokami, Masashi
- Kartal, Ece
- Schmidt, Thomas S.B.
- Estudillo, Lidia
- Trebicka, Jonel
- Kersting, Stephan
- Langheinrich, Melanie
- Uemura, Naomi
- Itoi, Takao
- Kawai, Takashi
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 2022-07
- Volume
- 163
- Issue
- 1
- Pages
- 222-238
- ISSN
- 0016-5085 (ISSN-L)
- OpenAlex
- W4223560232
- Cited by
- 209
- References
- 64
- Citations by year
- 2026: 36 · 2025: 54 · 2024: 66 · 2023: 40 · 2022: 13
- FWCI
- 14.28
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Gastroenterology (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science
- Smoking Research Foundation
- Government of Japan Ministry of Health Labour and Welfare
- Takeda Science Foundation
- Uehara Memorial Foundation
- National Center for Global Health and Medicine
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Keywords
- pancreatic ductal carcinoma, gut microbiota, oral microbiota, cancer prediction, dysbiosis, Streptococcus, Veillonella, Faecalibacterium prausnitzii, bacteriophages, cross-cohort validation
- MeSH terms
- Feces, Humans, Pancreatic Neoplasms, Prospective Studies, Metagenome, Metagenomics, Dysbiosis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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