Preliminary Comparison of Oral and Intestinal Human Microbiota in Patients with Colorectal Cancer: A Pilot Study

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Abstract

In this study Next-Generation Sequencing (NGS) was used to analyze and compare human microbiota from three different compartments, i.e., saliva, feces, and cancer tissue (CT), of a selected cohort of 10 Italian patients with colorectal cancer (CRC) vs. 10 healthy controls (saliva and feces). Furthermore, the Fusobacterium nucleatum abundance in the same body site was investigated through real-time quantitative polymerase chain reaction (qPCR) to assess the association with CRC. Differences in bacterial composition, F. nucleatum abundance in healthy controls vs. CRC patients, and the association of F. nucleatum with clinical parameters were observed. Taxonomic analysis based on 16S rRNA gene, revealed the presence of three main bacterial phyla, which includes about 80% of reads: Firmicutes (39.18%), Bacteroidetes (30.36%), and Proteobacteria (10.65%). The results highlighted the presence of different bacterial compositions; in particular, the fecal samples of CRC patients seemed to be enriched with Bacteroidetes, whereas in the fecal samples of healthy controls Firmicutes were one of the major phyla detected though these differences were not statistically significant. The CT samples showed the highest alpha diversity values. These results emphasize a different taxonomic composition of feces from CRC compared to healthy controls. Despite the low number of samples included in the study, these results suggest the importance of microbiota in the CRC progression and could pave the way to the development of therapeutic interventions and novel microbial-related diagnostic tools in CRC patients.

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Bacterial diversity in the oral cavity of 10 healthy individuals.

Elisabeth Bik, Clara Long, Gary Armitage … (2010)

The composition of the oral microbiota from 10 individuals with healthy oral tissues was determined using culture-independent techniques. From each individual, 26 specimens, each from different oral sites at a single point in time, were collected and pooled. An 11th pool was constructed using portions of the subgingival specimens from all 10 individuals. The 16S ribosomal RNA gene was amplified using broad-range bacterial primers, and clone libraries from the individual and subgingival pools were constructed. From a total of 11,368 high-quality, nonchimeric, near full-length sequences, 247 species-level phylotypes (using a 99% sequence identity threshold) and 9 bacterial phyla were identified. At least 15 bacterial genera were conserved among all 10 individuals, with significant interindividual differences at the species and strain level. Comparisons of these oral bacterial sequences with near full-length sequences found previously in the large intestines and feces of other healthy individuals suggest that the mouth and intestinal tract harbor distinct sets of bacteria. Co-occurrence analysis showed significant segregation of taxa when community membership was examined at the level of genus, but not at the level of species, suggesting that ecologically significant, competitive interactions are more apparent at a broader taxonomic level than species. This study is one of the more comprehensive, high-resolution analyses of bacterial diversity within the healthy human mouth to date, and highlights the value of tools from macroecology for enhancing our understanding of bacterial ecology in human health.

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Fusobacterium nucleatum associates with stages of colorectal neoplasia development, colorectal cancer and disease outcome.

L. Flanagan, J. Schmid, M. Ebert … (2014)

Commensal bacteria in the colon may play a role in colorectal cancer (CRC) development. Recent studies from North America showed that Fusobacterium nucleatum (Fn) infection is over-represented in disease tissue versus matched normal tissue in CRC patients. Using quantitative real-time polymerase chain reaction (qPCR) of DNA extracted from colorectal tissue biopsies and surgical resections of three European cohorts totalling 122 CRC patients, we found an over-abundance of Fn in cancerous compared to matched normal tissue (p < 0.0001). To determine whether Fn infection is an early event in CRC development, we assayed Fn in colorectal adenoma (CRA) tissue from 52 Irish patients. While for all CRAs the Fn level was not statistically significantly higher in disease versus normal tissue (p = 0.06), it was significantly higher for high-grade dysplasia (p = 0.015). As a secondary objective, we determined that CRC patients with low Fn levels had a significantly longer overall survival time than patients with moderate and high levels of the bacterium (p = 0.008). The investigation of Fn as a potential non-invasive biomarker for CRC screening showed that, while Fn was more abundant in stool samples from CRC patients compared to adenomas or controls, the levels in stool did not correlate with cancer or adenoma tissue levels from the same individuals. This is the first study examining Fn in the colonic tissue and stool of European CRC and CRA patients, and suggests Fn as a novel risk factor for disease progression from adenoma to cancer, possibly affecting patient survival outcomes. Our results highlight the potential of Fn detection as a diagnostic and prognostic determinant in CRC patients.

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Fusobacterium Is Associated with Colorectal Adenomas

Amber McCoy, Félix Araujo-Pérez, Andrea Azcárate-Peril … (2013)

The human gut microbiota is increasingly recognized as a player in colorectal cancer (CRC). While particular imbalances in the gut microbiota have been linked to colorectal adenomas and cancer, no specific bacterium has been identified as a risk factor. Recent studies have reported a high abundance of Fusobacterium in CRC subjects compared to normal subjects, but this observation has not been reported for adenomas, CRC precursors. We assessed the abundance of Fusobacterium species in the normal rectal mucosa of subjects with (n = 48) and without adenomas (n = 67). We also confirmed previous reports on Fusobacterium and CRC in 10 CRC tumor tissues and 9 matching normal tissues by pyrosequencing. We extracted DNA from rectal mucosal biopsies and measured bacterial levels by quantitative PCR of the 16S ribosomal RNA gene. Local cytokine gene expression was also determined in mucosal biopsies from adenoma cases and controls by quantitative PCR. The mean log abundance of Fusobacterium or cytokine gene expression between cases and controls was compared by t-test. Logistic regression was used to compare tertiles of Fusobacterium abundance. Adenoma subjects had a significantly higher abundance of Fusobacterium species compared to controls (p = 0.01). Compared to the lowest tertile, subjects with high abundance of Fusobacterium were significantly more likely to have adenomas (OR 3.66, 95% CI 1.37–9.74, p-trend 0.005). Cases but not controls had a significant positive correlation between local cytokine gene expression and Fusobacterium abundance. Among cases, the correlation for local TNF-α and Fusobacterium was r = 0.33, p = 0.06 while it was 0.44, p = 0.01 for Fusobacterium and IL-10. These results support a link between the abundance of Fusobacterium in colonic mucosa and adenomas and suggest a possible role for mucosal inflammation in this process.

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Contributors

Edda Russo: URI : http://loop.frontiersin.org/people/512121/overview

Giovanni Bacci: URI : http://loop.frontiersin.org/people/321263/overview

Carolina Chiellini: URI : http://loop.frontiersin.org/people/360397/overview

Camilla Fagorzi: URI : http://loop.frontiersin.org/people/477609/overview

Elena Niccolai: URI : http://loop.frontiersin.org/people/485201/overview

Antonio Taddei: URI : http://loop.frontiersin.org/people/438595/overview

Federica Ricci: URI : http://loop.frontiersin.org/people/509029/overview

Maria N. Ringressi: URI : http://loop.frontiersin.org/people/471213/overview

Manouela Miloeva: URI : http://loop.frontiersin.org/people/512613/overview

Alessio Mengoni: URI : http://loop.frontiersin.org/people/107432/overview

Renato Fani: URI : http://loop.frontiersin.org/people/131710/overview

Amedeo Amedei: URI : http://loop.frontiersin.org/people/43972/overview

Journal

Journal ID (nlm-ta): Front Microbiol

Journal ID (iso-abbrev): Front Microbiol

Journal ID (publisher-id): Front. Microbiol.

Title: Frontiers in Microbiology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-302X

Publication date (Electronic): 12 January 2018

Publication date Collection: 2017

Volume: 8

Electronic Location Identifier: 2699

Affiliations

[1] ¹Immunology, Department of Clinical and Experimental Medicine, University of Florence , Florence, Italy

[2] ²Department of Biology, University of Florence , Florence, Italy

[3] ³Department of Surgery and Translational Medicine, University of Florence , Florence, Italy

[4] ⁴Neuromusculoskeletal Department (Interdisciplinary Internal Medicine), Azienda Ospedaliera Universitaria Careggi , Florence, Italy

Author notes

Edited by: Malka Halpern, University of Haifa, Israel

Reviewed by: Carlotta De Filippo, Consiglio Nazionale Delle Ricerche (CNR), Italy; Nick Stephen Jakubovics, Newcastle University, United Kingdom; Eija Könönen, University of Turku, Finland

*Correspondence: Amedeo Amedei amedeo.amedei@ 123456unifi.it

This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology

Article

DOI: 10.3389/fmicb.2017.02699

PMC ID: 5770402

PubMed ID: 29375539

SO-VID: 04e75276-8098-4e8b-a7a7-bffea6dc841f

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 01 June 2017

Date accepted : 26 December 2017

Page count

Figures: 7, Tables: 1, Equations: 0, References: 65, Pages: 13, Words: 8026

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Preliminary Comparison of Oral and Intestinal Human Microbiota in Patients with Colorectal Cancer: A Pilot Study

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Tick microbiome

Most cited references 27

Bacterial diversity in the oral cavity of 10 healthy individuals.

Fusobacterium nucleatum associates with stages of colorectal neoplasia development, colorectal cancer and disease outcome.

Fusobacterium Is Associated with Colorectal Adenomas

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Cited by 52

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