Alterations in Enteric Virome Are Associated With Colorectal Cancer and Survival Outcomes
Open accessAbstract
Background & Aims Patients with colorectal cancer (CRC) have a different gut microbiome signature than individuals without CRC. Little is known about the viral component of CRC-associated microbiome. We aimed to identify and validate viral taxonomic markers of CRC that might be used in detection of the disease or predicting outcome. Methods We performed shotgun metagenomic analyses of viromes of fecal samples from 74 patients with CRC (cases) and 92 individuals without CRC (controls) in Hong Kong (discovery cohort). Viral sequences were classified by taxonomic alignment against an integrated microbial reference genome database. Viral markers associated with CRC were validated using fecal samples from 3 separate cohorts: 111 patients with CRC and 112 controls in Hong Kong, 46 patients with CRC and 63 controls in Austria, and 91 patients with CRC and 66 controls in France and Germany. Using abundance profiles of CRC-associated virome genera, we constructed random survival forest models to identify those associated with patient survival times. Results The diversity of the gut bacteriophage community was significantly increased in patients with CRC compared with controls. Twenty-two viral taxa discriminated cases from controls with an area under the receiver operating characteristic curve of 0.802 in the discovery cohort. The viral markers were validated in 3 cohorts, with area under the receiver operating characteristic curves of 0.763, 0.736, and 0.715, respectively. Clinical subgroup analysis showed that dysbiosis of the gut virome was associated with early- and late-stage CRC. A combination of 4 taxonomic markers associated with reduced survival of patients with CRC (log-rank test, P = 8.1 × 10 –6 ) independently of tumor stage, lymph node metastases, or clinical parameters. We found altered interactions between bacteriophages and oral bacterial commensals in fecal samples from patients with CRC compared with controls. Conclusions In a metagenomic analysis of fecal samples from patients and controls, we identified virome signatures associated with CRC. These data might be used to develop tools to identify individuals with CRC or predict outcomes.
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Enrichment of bacterial species from oral cavity is characteristic of CRC GOMS, along with enrichment in invasive polymicrobial bacterial biofilms in patients with right-sided tumours.
“The enrichment of bacterial species from the oral cavity is characteristic of the CRC GOMS50,76–79, along with an enrichment in invasive polymicrobial bacterial biofilms in patients with right-sided tumours76,80,81.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [79]
Studies discovered specific virome and mycobiome signatures for CRC GOMS, and in vitro and in vivo experiments showed Aspergillus rambellii can promote CRC cell growth.
“Studies have discovered specific virome79 and mycobiome86,87 signatures for CRC GOMS, and included in vitro and in vivo experiments showing that the fungus Aspergillus rambellii can promote CRC cell growth86.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [79]
The enteric virome and mycobiome have been linked with colorectal cancer.
“The enteric virome and mycobiome (fungal microbiome) have also been linked with CRC.72–74”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [72]
Compared with controls, colorectal cancer cases had increased diversity in bacteriophage viromes, associated with reduced bacterial diversity, and modest enrichment of specific viral taxa such as Inovirus and Tunalikevirus.
“Compared to controls, CRC cases had increased diversity in bacteriophage viromes, associated with reduced bacterial diversity, and modest enrichment of specific viral taxa, such as members of Inovirus and Tunalikevirus, whose bacterial hosts have been implicated in CRC”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [72]
These findings indicate an interaction between the virome and bacteriome in colorectal cancer risk.
“These findings indicate an interaction between the virome and bacteriome in risk of CRC.72, 74”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [72]
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- Authors
- Nakatsu, G., Zhou, H., Wu, W. K. K., Wong, S. H., Coker, O. O., Dai, Z., Li, X., Szeto, C.-H., Sugimura, N., Lam, T. Y.-T., Yu, A. C.-S., Wang, X., Chen, Z., Wong, M. C.-S., Ng, S. C., Chan, M. T. V., Chan, P. K. S., Chan, F. K. L., Sung, J. J.-Y., & Yu, J.
- Affiliations
- Chinese University of Hong Kong (HK)
- Corresponding author
- Yu, Jun
- ORCID
- Nakatsu, Geicho
- Zhou, Haokui
- Wu, William Ka Kei
- Wong, Sunny Hei
- Coker, Olabisi Oluwabukola
- Li, Xiangchun
- Szeto, Chun-Ho
- Lam, Thomas Yuen-Tung
- Yu, Allen Chi-Shing
- Wang, Xiansong
- Chen, Zigui
- Wong, Martin Chi-Sang
- Ng, Siew Chien
- Chan, Matthew Tak Vai
- Chan, Paul Kay Sheung
- Chan, Francis Ka Leung
- Sung, Joseph Jao-Yiu
- Yu, Jun
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 2018-08
- Volume
- 155
- Issue
- 2
- Pages
- 529-541.e5
- ISSN
- 0016-5085 (ISSN-L)
- OpenAlex
- W2800015127
- Cited by
- 386
- References
- 88
- Citations by year
- 2026: 33 · 2025: 40 · 2024: 50 · 2023: 72 · 2022: 65 · 2021: 56 · 2020: 37 · 2019: 25 · 2018: 6
- FWCI
- 23.32
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Gastroenterology (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Keywords
- colorectal cancer, gut virome, bacteriophages, viral markers, cancer detection, survival prediction, fecal microbiota, dysbiosis, viral-bacterial interactions, tumor stage, lymph node metastasis
- MeSH terms
- Gastrointestinal Microbiome, Austria, Colonoscopy, Cross-Sectional Studies, Feces, Female, France, Germany, Hong Kong, Humans, Male, Middle Aged, Sensitivity and Specificity, Biomarkers, Tumor, Viruses, Colorectal Neoplasms, Cohort Studies, Survival Analysis, Case-Control Studies, Metagenomics, Dysbiosis
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