Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma
Open accessAbstract
Background Accumulating evidence indicates that diet is one of the most important environmental factors involved in the progression from advanced colorectal adenoma (A-CRA) to colorectal cancer.Objective We evaluated the possible effects of dietary fiber on the fecal microbiota of patients with A-CRA.Design Patients with a diagnosis of A-CRA by pathological examination were enrolled in the A-CRA group. Patients with no obvious abnormalities or histopathological changes were enrolled in the healthy control (HC) group. Dietary fiber intake was assessed in all patients. Short-chain fatty acids (SCFAs) in feces were detected by gas chromatography. The fecal microbiota community was analyzed by 454 pyrosequencing based on 16S ribosomal RNA.Results Lower dietary fiber patterns and consistently lower SCFA production were observed in the A-CRA group (n = 344). Principal component analysis showed distinct differences in the fecal microbiota communities of the 2 groups. Clostridium, Roseburia, and Eubacterium spp. were significantly less prevalent in the A-CRA group (n = 47) than in the HC group (n = 47), whereas Enterococcus and Streptococcus spp. were more prevalent in the A-CRA group (n = 47) (all P < 0.05). Butyrate and butyrate-producing bacteria were more prevalent in a subgroup of HC subjects with a high fiber intake than in those in both the low-fiber HC subgroup and the high-fiber A-CRA subgroup (all P < 0.05).Conclusion A high-fiber dietary pattern and subsequent consistent production of SCFAs and healthy gut microbiota are associated with a reduced risk of A-CRA. This trial was registered at www.chictr.org as ChiCTR-TRC-00000123.
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Some but not all cross-sectional studies associated higher fiber intake with increased fecal short-chain fatty acid levels and enrichment of short-chain fatty acid-producing bacteria such as Eubacterium rectale, Roseburia spp., and Faecalibacterium prausnitzii.
“Some but not all cross-sectional studies associated higher fiber intake with increased fecal levels of SCFAs and enrichment of SCFA-producing bacteria, such as Eubacterium rectale, Roseburia spp., and Faecalibacterium prausnitzii.126, 127”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [127]
Cites
Jemal, A., Bray, F., Ferlay, J., Ward, E., & Forman, D. (2011) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.20107 · Cited by 54,708 · see citing works
Diversity of the Human Intestinal Microbial Flora
Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S. R., Nelson, K. E., & Relman, D. A. (2005) · Science · doi:10.1126/science.1110591 · Cited by 7,913 · see citing works
Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J., & Glöckner, F. O. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm864 · Cited by 6,682 · see citing works
Colonic Health: Fermentation and Short Chain Fatty Acids
Wong, J. M. W., de Souza, R., Kendall, C. W. C., Emam, A., & Jenkins, D. J. A. (2006) · Journal of Clinical Gastroenterology · doi:10.1097/00004836-200603000-00015 · Cited by 2,739 · see citing works
Louis, P., & Flint, H. J. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01514.x · Cited by 2,179 · see citing works
Regulation of short-chain fatty acid production
Macfarlane, S., & Macfarlane, G. T. (2003) · Proceedings of the Nutrition Society · doi:10.1079/pns2002207 · Cited by 1,939 · see citing works
Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers
Wang, T., Cai, G., Qiu, Y., Fei, N., Zhang, M., Pang, X., Jia, W., Cai, S., & Zhao, L. (2012) · The ISME Journal · doi:10.1038/ismej.2011.109 · Cited by 1,287 · see citing works
Symbiotic gut microbes modulate human metabolic phenotypes
Li, M., Wang, B., Zhang, M., Rantalainen, M., Wang, S., Zhou, H., Zhang, Y., Shen, J., Pang, X., Zhang, M., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712038105 · Cited by 1,144 · see citing works
Bingham, S. A., Day, N., Luben, R., Ferrari, P., Slimani, N., Norat, T., Clavel‐Chapelon, F., Kesse‐Guyot, E., Nieters, A., Boeing, H., et al. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13174-1 · Cited by 1,109 · see citing works
Characterization of fecal microbial communities in patients with liver cirrhosis
Chen, Y., Yang, F., Lu, H., Wang, B., Chen, Y., Lei, D., Wang, Y., Zhu, B., & Li, L. (2011) · Hepatology · doi:10.1002/hep.24423 · Cited by 1,038 · see citing works
Human Intestinal Lumen and Mucosa-Associated Microbiota in Patients with Colorectal Cancer
Chen, W., Liu, F., Ling, Z., Tong, X., & Xiang, C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039743 · Cited by 1,029 · see citing works
Self-citationDuncan, S. H., Belenguer, A., Holtrop, G., Johnstone, A. M., Flint, H. J., & Lobley, G. E. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.02340-06 · Cited by 941 · see citing works
Prentice, R. L., Caan, B., Chlebowski, R. T., Patterson, R., Kuller, L. H., Ockene, J. K., Margolis, K. L., Limacher, M. C., Manson, J. E., Parker, L. M., et al. (2006) · JAMA · doi:10.1001/jama.295.6.629 · Cited by 828 · see citing works
Ramirez-Farias, C., Slezak, K., Fuller, Z., Duncan, A., Holtrop, G., & Louis, P. (2008) · British Journal of Nutrition · doi:10.1017/s0007114508019880 · Cited by 822 · see citing works
Louis, P., Young, P., Holtrop, G., & Flint, H. J. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.02066.x · Cited by 783 · see citing works
Glade, M. J. (1999) · Nutrition · doi:10.1016/s0899-9007(99)00021-0 · Cited by 778 · see citing works
Colon Cancer: A Review of the Epidemiology
Potter, J. D., Slattery, M. L., Bostick, R. M., & Gapstur, S. M. (1993) · Epidemiologic Reviews · doi:10.1093/oxfordjournals.epirev.a036132 · Cited by 767 · see citing works
Dietary Fiber and the Risk of Colorectal Cancer and Adenoma in Women
Fuchs, C. S., Giovannucci, E. L., Colditz, G. A., Hunter, D. J., Stampfer, M. J., ROSNER, B. A., Speizer, F. E., & Willett, W. C. (1999) · New England Journal of Medicine · doi:10.1056/nejm199901213400301 · Cited by 668 · see citing works
Louis, P., Duncan, S. H., McCrae, S. I., Millar, J., Jackson, M. S., & Flint, H. J. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.7.2099-2106.2004 · Cited by 517 · see citing works
Manning, T. S., & Gibson, G. R. (2004) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2003.10.008 · Cited by 480 · see citing works
Low-Fat Dietary Pattern and Risk of Colorectal Cancer
Beresford, S. A. A., Johnson, K., Ritenbaugh, C., Lasser, N. L., Snetselaar, L. G., Black, H. R., Anderson, G. L., Assaf, A. R., Bassford, T. L., Bowen, D. J., et al. (2006) · JAMA · doi:10.1001/jama.295.6.643 · Cited by 402 · see citing works
Energy balance and colon cancer--beyond physical activity.
Ml, S., Potter, J. D., Caan, B. J., Edwards, S. L., Coates, A. O., Ma, K.-N., & Td, B. (1997) · PubMed · Cited by 386 · see citing works
Scharlau, D., Borowicki, A., Habermann, N., Hofmann, T., Klenow, S., Miene, C., Munjal, U., Stein, K., & Glei, M. (2009) · Mutation research · doi:10.1016/j.mrrev.2009.04.001 · Cited by 346 · see citing works
Human Colonic Microbiota: Ecology, Physiology and Metabolic Potential of Intestinal Bacteria
Macfarlane, G. T., & Macfarlane, S. (1997) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365521.1997.11720708 · Cited by 342 · see citing works
Parallel tagged sequencing on the 454 platform
Meyer, M., Stenzel, U., & Hofreiter, M. (2008) · Nature Protocols · doi:10.1038/nprot.2007.520 · Cited by 324 · see citing works
A High-Throughput DNA Sequence Aligner for Microbial Ecology Studies
Schloss, P. D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008230 · Cited by 320 · see citing works
Winawer, S. J., Zauber, A. G., Fletcher, R. H., et al. (2006) · CA A Cancer Journal for Clinicians · doi:10.3322/canjclin.56.3.143 · Cited by 303 · see citing works
Devillard, E., McIntosh, F. M., Duncan, S. H., & Wallace, R. J. (2007) · Journal of Bacteriology · doi:10.1128/jb.01359-06 · Cited by 285 · see citing works
Cultivable bacterial diversity from the human colon
Duncan, S. H., Louis, P., & Flint, H. J. (2007) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2007.02129.x · Cited by 279 · see citing works
Overvad, K., Tjønneland, A. M., Haraldsdóttir, J., Ewertz, M., & Jensen, O. M. (1991) · International Journal of Epidemiology · doi:10.1093/ije/20.4.900 · Cited by 248 · see citing works
The butyrate story: old wine in new bottles?
Scheppach, W. M., & Weiler, F. (2004) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/00075197-200409000-00009 · Cited by 246 · see citing works
Mucosa-Associated Bacterial Diversity in Relation to Human Terminal Ileum and Colonic Biopsy Samples
Ahmed, S., Macfarlane, G. T., Fite, A., McBain, A. J., Gilbert, P., & Macfarlane, S. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01143-07 · Cited by 227 · see citing works
Targeted high-throughput sequencing of tagged nucleic acid samples
Meyer, M., Stenzel, U., Myles, S., Prüfer, K., & Hofreiter, M. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm566 · Cited by 194 · see citing works
Microbial and viral pathogens in colorectal cancer
Collins, D., Hogan, A. M., & Winter, D. C. (2010) · The Lancet Oncology · doi:10.1016/s1470-2045(10)70186-8 · Cited by 172 · see citing works
Butyrate enemas in experimental colitis and protection against large bowel cancer in a rat model
D’Argenio, G., Cosenza, V., Cave, M. D., Iovino, P., Valle, N. D., Lombardi, G., & Mazzacca, G. (1996) · Gastroenterology · doi:10.1053/gast.1996.v110.pm8964397 · Cited by 136 · see citing works
Lin, J. Y., Zhang, S. M., Cook, N. R., Rexrode, K. M., Liu, S., Manson, J. E., Lee, I.-M. M., & Buring, J. E. (2005) · Cancer Causes & Control · doi:10.1007/s10552-004-4025-1 · Cited by 117 · see citing works
Tjønneland, A. M., Haraldsdóttir, J., Overvad, K., et al. (1992) · International Journal of Epidemiology · doi:10.1093/ije/21.4.770 · Cited by 117 · see citing works
Fruit and vegetable intake and prevalence of colorectal adenoma in a cancer screening trial
Millen, A. E., Subar, A. F., Graubard, B. I., Peters, U., Hayes, R. B., Weissfeld, J. L., Yokochi, L. A., & Ziegler, R. G. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.5.1754 · Cited by 112 · see citing works
Colorectal cancer incidence trends by subsite in urban Shanghai, 1972-1994.
Ji, B., Devesa, S. S., Chow, W. H., et al. (1998) · PubMed · Cited by 109 · see citing works
Diet and colorectal cancer prevention
Bingham, S. A. (2000) · Biochemical Society Transactions · doi:10.1042/bst0280012 · Cited by 104 · see citing works
Fruit and vegetable intake and prevalence of colorectal adenoma in a cancer screening trial
Millen, A. E., Subar, A. F., Graubard, B. I., et al. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.6.1754 · Cited by 61 · see citing works
Fecal short-chain fatty acid (SCFA) analysis by capillary gas-liquid chromatography
Scheppach, W. M., Fabian, C., & Kasper, H. (1987) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/46.4.641 · Cited by 37 · see citing works
Folic acid and sodium butyrate prevent tumorigenesis in a mouse model of colorectal cancer
Lu, R., Wang, X., Sun, D.-F., Tian, X.-Q., Zhao, S.-L., Chen, Y., & Fang, J. (2008) · Epigenetics · doi:10.4161/epi.3.6.7125 · Cited by 30 · see citing works
Self-citationProximal shift of advanced adenomas in the large bowel – does it really exist?
Kiedrowski, M., Mróz, A., Kaminski, M. F., et al. (2012) · Polskie Archiwum Medycyny Wewnętrznej · doi:10.20452/pamw.1275 · Cited by 6 · see citing works
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Singh, R. K., Chang, H.-W., Yan, D., Lee, K. M., Ucmak, D., Wong, K., Abrouk, M., Farahnik, B., Nakamura, M., Zhu, T. H., et al. (2017) · Journal of Translational Medicine · doi:10.1186/s12967-017-1175-y · Cited by 2,599 · see citing works
Fusobacterium nucleatum Promotes Chemoresistance to Colorectal Cancer by Modulating Autophagy
Yu, T., Guo, F., Yu, Y., Sun, T., Ma, D., Han, J., Qian, Y., Kryczek, I., Sun, D., Nagarsheth, N., et al. (2017) · Cell · doi:10.1016/j.cell.2017.07.008 · Cited by 2,198 · see citing works
Self-citationCurrent Understanding of Dysbiosis in Disease in Human and Animal Models
DeGruttola, A. K., Low, D., Mizoguchi, A., & Mizoguchi, E. (2016) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000750 · Cited by 1,122 · see citing works
Diet, microorganisms and their metabolites, and colon cancer
O'Keefe, S. J. D. (2016) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.165 · Cited by 1,100 · see citing works
Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer
Song, M., Chan, A. T., & Sun, J. (2020) · Gastroenterology · doi:10.1053/j.gastro.2019.06.048 · Cited by 752 · see citing works
Nutrients, foods, and colorectal cancer prevention
Song, M., Garrett, W. S., & Chan, A. T. (2015) · Gastroenterology · doi:10.1053/j.gastro.2014.12.035 · Cited by 700 · see citing works
Sex, body mass index, and dietary fiber intake influence the human gut microbiome
Dominianni, C., Sinha, R., Goedert, J. J., Pei, Z., Yang, L., Hayes, R. B., & Ahn, J. (2015) · PLOS ONE · doi:10.1371/journal.pone.0124599 · Cited by 468 · see citing works
Self-citationHibberd, A. A., Lyra, A., Ouwehand, A. C., Rolny, P., Lindegren, H., Cedgård, L., & Wettergren, Y. (2017) · BMJ Open Gastroenterology · doi:10.1136/bmjgast-2017-000145 · Cited by 373 · see citing works
Immune regulation by microbiome metabolites
Kim, C. H. (2018) · Immunology · doi:10.1111/imm.12930 · Cited by 375 · see citing works
Baxter, N. T., Ruffin, M. T., Rogers, M. A. M., & Schloss, P. D. (2016) · Genome Medicine · doi:10.1186/s13073-016-0290-3 · Cited by 354 · see citing works
Mehta, R. S., Nishihara, R., Cao, Y., Song, M., Mima, K., Qian, Z. R., Nowak, J. A., Kosumi, K., Hamada, T., Masugi, Y., et al. (2017) · JAMA Oncology · doi:10.1001/jamaoncol.2016.6374 · Cited by 325 · see citing works
Lindefeldt, M., Eng, A., Darban, H., Bjerkner, A., Zetterström, C. K., Allander, T., Andersson, B., Borenstein, E., Dahlin, M., & Prast-Nielsen, S. (2019) · npj Biofilms and Microbiomes · doi:10.1038/s41522-018-0073-2 · Cited by 310 · see citing works
Baxter, N. T., Zackular, J. P., Chen, G. Y., & Schloss, P. D. (2014) · Microbiome · doi:10.1186/2049-2618-2-20 · Cited by 299 · see citing works
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- Authors
- Chen, H.-M., Yu, Y.-N., Wang, J.-L., Lin, Y.-W., Kong, X., Yang, C.-Q., Yang, L., Liu, Z.-J., Yuan, Y.-Z., Liu, F., Wu, J.-X., Zhong, L., Fang, D.-C., Zou, W., & Fang, J.-Y.
- Affiliations
- Shanghai Jiao Tong University (CN)
- Tongji University (CN)
- Fudan University (CN)
- Army Medical University (CN)
- Venue
- The American Journal of Clinical Nutrition
- Publisher
- Elsevier BV
- Published
- 2013-05
- Volume
- 97
- Issue
- 5
- Pages
- 1044-1052
- ISSN
- 0002-9165 (ISSN-L)
- OpenAlex
- W2166066205
- Cited by
- 321
- References
- 44
- Citations by year
- 2026: 14 · 2025: 17 · 2024: 25 · 2023: 38 · 2022: 38 · 2021: 20 · 2020: 33 · 2019: 21 · 2018: 30 · 2017: 27 · 2016: 20 · 2015: 18 · 2014: 14 · 2013: 5
- FWCI
- 8.50
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- American Journal of Clinical Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
- Keywords
- advanced adenoma, dietary fiber intake, gut microbiota, short-chain fatty acids, butyrate, butyrate-producing bacteria, colorectal cancer risk, fecal microbiota composition, Clostridium, Roseburia, Enterococcus, Streptococcus
- MeSH terms
- Aged, Butyrates, China, Chromatography, Gas, Cross-Sectional Studies, Diet, Dietary Fiber, DNA, Bacterial, Fatty Acids, Volatile, Feces, Female, Gram-Positive Bacteria, Humans, Life Style, Male, Middle Aged, Surveys and Questionnaires, RNA, Ribosomal, 16S, Colorectal Neoplasms, Multivariate Analysis, Logistic Models, Case-Control Studies, Sequence Analysis, DNA, Gastrointestinal Tract, Metagenome
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